Focal Philophthalmus gralli infection possibly persists in Melanoides tuberculata over two years following the definitive hosts' removal

Philophthalmosis is a zoonotic disease associated largely with the spread of the invasive freshwater snail Melanoides tuberculata, serving as an intermediate host. Here we examined Philophthalmus gralli focal fenced infection site reported recently as being associated with Tinamus major and M. tuberculata in Alajuela, Costa Rica. Removal of the definitive hosts allowed us to address also the long-term survival strategy of the parasite. Initially, the snail intermediate hosts displayed high prevalence of P. gralli infection across all its age cohorts. Two years following the removal of definitive hosts, the infection rate decreased by one order of magnitude, while the snails aging less than one year displayed zero infection prevalence. Additionally, phylogenetic analysis of mitochondrial (ND1) and nuclear (ITS1, ITS2) DNA loci revealed negligible intrasite DNA variability of the specimens obtained at the study site in Costa Rica (but not of those obtained earlier in Peru or New Zealand), supporting strongly the hypothesis on focal origin of the infection. The observed dynamics of infection suggests the explanation for the high variability in P. gralli prevalence in intermediate hosts experienced worldwide. We noticed that the reports claiming > 20% prevalence of M. tuberculata infection by P. gralli originated exclusively from foci with known eye infection of the definitive hosts, while the P. gralli infection penetrance < 2% is typically associated with sites, where the infection of definitive hosts was not observed, suggesting that the infected definitive hosts were present onsite only in the past, or were present only at a site upstream or downstream of the respective sampling site. Thus, this is the first evidence on the possible persistence of eye-trematode infection site for over two years following the last confirmed outbreak in its adult hosts.     

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).     

An outbreak of philophthalmosis in Larus michahellis and Larus fuscus gulls in Iberian Peninsula

Trematodes of the genus Philophthalmus Loos, 1899 are the eye parasites of birds and mammals, which use freshwater snails as their first intermediate hosts. Here we examined the presence of philophthalmids in a total of 1515 gulls (589 Larus fuscus and 926 Larus michahellis) admitted between January 2010 and October 2016 for rehabilitation at Olhão (Portugal), by the use of combined morphological and molecular analysis. We recorded the first infected L. fuscus and L. michahellis in July and November 2015, respectively. The philophthalmids were located in the conjunctival sac or under the nictitating membrane. Gulls infected with Philophthalmus lucipetus Rudolphi, 1819 presented no clinical signs, while those infected with Philophthalmus lacrymosus Braun, 1902 presented serious eye damage in the same host species. The prevalence of P. lucipetus reached 3.6% in L. fuscus and 0.8% in L. michahellis; the prevalence of P. lacrymosus reached 0.3% and 0.0%, respectively. The outbreak of P. lucipetus likely started in a narrowly defined area, since the first six cases, found between July and October 2015, originated from a single municipality, and only later more cases started to be retrieved from other municipalities of Portugal. These findings represent the first records of both philophthalmids in the Iberian Peninsula, their first records in L. michahellis and the first record of P. lacrymosus in L. fuscus. Further follow-up of the outbreak and the identification of intermediate hosts are needed.     

Resistance of an invasive gastropod to an indigenous trematode parasite in Lake Malawi

Successful establishment and spread of biological invaders may be promoted by the absence of population-regulating enemies such as pathogens, parasites or predators. This may come about when introduced taxa are missing enemies from their native habitats, or through immunity to enemies within invaded habitats. Here we provide field evidence that trematode parasites are absent in a highly invasive morph of the gastropod Melanoides tuberculata in Lake Malawi, and that the invasive morph is resistant to indigenous trematodes that castrate and induce gigantism in native M. tuberculata. Since helminth infections can strongly influence host population abundances in other host-parasite systems, this enemy release may have provided an advantage to the invasive morph in terms of reproductive capacity and survivorship.     

Population dynamics of Melanoides tuberculata (Thiaridae) snails in a desert spring,United Arab Emirates and infection with larval trematodes

A dense population of Melanoides tuberculata was found at a brackish (5.93–6.98%) desert spring in the United Arab Emirates. A total of 232–300 snails were measured and examined for larval trematodes during the period January 1990 to January 1991. The relative abundance of various size classes of the snail has shown that the mass release of young snails occurred twice a year, in April–May and September–October. Seven different forms of cercariae were found: A xiphidiocercaria, a brevifurcate cercaria, two pleurolophocercous cercariae, two gymnocephalous cercariae, and the cercaria of Philophthalmus gralli. The overall infection rate of this snail was 73.6% and ranged from 51.3 during February–March 1990 to 91.7% during January 1991. The xiphidiocercaria and the P. gralli cercaria were the most abundant and were found in 21.1% and 29.7%, respectively, of the examined snails. A relatively high rate (9.5%) of double infection was found. Cases of triple infection were also encountered.     

First report of Melanoides tuberculata (Mollusca: Thiaridae) harboring a xiphidiocercaria in Brazil: A new parasite introduced in the Americas?

Xiphidiocercariae were found in the invasive snail Melanoides tuberculata collected during a malacological survey in Ceará-Mirim, State of Rio Grande do Norte, Northeastern Brazil in November 2018 and submitted to morphological and molecular analyses. The morphology revealed similarities between the larvae here reported for the first time in M. tuberculata from Brazil and other xiphidiocercariae described in thiarid snails from Asia and Africa. Phylogenetic analyses based on 28S and ITS-2 sequences revealed that the larvae correspond to an unidentified species of the family Lecithodendriidae. Aspects related to the morphology and taxonomy of xiphidiocercariae found in M. tuberculata are briefly discussed. It is possible that the parasite here reported is a newly introduced species transmitted by M. tuberculata in the American continent.     

Interaction between the intermediate host of Fascioliasis in Tunisia,Galba truncatula and a possible competitor,Melanoides tuberculata (Muller, 1774): a field study

The snail Melanoides tuberculata has been used successfully in the control of some snails, intermediate host of parasitosis. Melanoides tuberculata has been found in Tunisia, but its effects on populations of native snail have not yet been evaluated in the field. Our objective is to determine whether M. tuberculata competed with Galba truncatula, using a field study. Twelve monthly investigations were carried out along an irrigation system in Ain Soltane's oasis (southwest of Tunisia). Here, we describe the population dynamics of G. truncatula with and without M. tuberculata in two stations: a witness pilot station (S1), in which the snail lives alone, and an experimental station (S2), where two species live together. The abundance of G. truncatula varied according to subsistence or not of M. tuberculata. The number of annual generations is higher in S1 (four generations) than S2 (two generations). In the absence of other molluscs or predators that can influence the density of G. truncatula and assuming that climatic factors are mitigated by the presence of an oasean microclimate, these results show that the mollusc M. tuberculata has a competition with the vector species of fluke.     

Molecular characterization of Oxyspirura mansoni and Philophthalmus gralli collected from the eyes of domestic chickens in Bangladesh

A variety of helminths have been found in domestic chickens in Bangladesh, but little is known about their gene sequences. Here, parasitic nematodes and trematodes were collected from the eyes of domestic chickens and analyzed for their morphological and morphometric characteristics, and characterized molecularly. The helminths were identified as Oxyspirura mansoni and Philophthalmus gralli. The ITS1 and ITS2 sequences of O. mansoni were 532 bp and 306 bp in length, respectively, and showed low identity (50.7–62.7%) with those of O. petrowi and O. conjunctivalis. Furthermore, the O. mansoni CO1 sequences (393 bp) showed five haplotypes (97.5–99.5% similarity) that formed a monophyletic clade. With respect to P. gralli, the ITS1 (452 bp) and ITS2 (736 bp) sequences showed 100% similarity with the reference sequences in GenBank. Both the ND1 and CO1 phylograms showed that P. gralli from Bangladesh, Costa Rica and Peru form a monophyletic clade, distinct from the clades of P. lucipetus and P. lacrymosus. Our data show that, Philophthalmus gralli isolates from Bangladesh, Costa Rica and Peru are genetically close to each other.     

Pathology and first report of natural eye infection with the trematode Philophthalmus gralli (Digenea,Philophthalmidae) in Tinamus major (Tinamiformes,Tinamidae), Costa Rica

The eye-fluke Philophthalmus gralli (Philophthalmidae Looss, 1899) was found in six birds known as great tinamous (Tinamus major) reared in a wild animal shelter located in Alajuela, Costa Rica. The birds presented conjunctival hyperemia, blepharitis, anorexia and weakness. Some of them suffered from unilateral blindness and ocular loss. After morphometric analysis, the specimens showed characteristics compatible with the digenean trematode P. gralli. The clinical signs of infection were resolved by manual removal of the adults, treatment with praziquantel and relocation into an environment without a natural water source. In order to determine if an ongoing cycle of this pathogen was present in the shelter, the habitat of the birds was inspected for the presence of infected intermediate hosts and contaminated water and objects. It was found that the snails Melanoides tuberculata acted as the intermediate host, and reared the infectious stages toward other animals, as shown by the reproduction of ocular philophthalmiasis in chickens artificially infected with excysted metacercaria. Moreover, three out of every ten snails found in the place were infected with rediae of P. gralli, raising the possibility of the dispersion of the parasite into new environments as well as the imminent zoonotic risk. The finding of P. gralli in Costa Rica is the first official report in Central America.     

Comparative host reaction to Angiostrongylus malaysiensis (Nematoda) in three species of snails

Infection with Angiostrongylus malaysiensis was studied by means of tissue squash preparations and histological sections in three species of Malaysian aquatic snails: Lymnaea rubiginosa, Physastra sumatrana, and Melanoides tuberculata. Development to the third stage occurred normally in L. rubiginosa. The biphasic tissue reaction in this snail was similar to that described in Biomphalaria glabrata infected with A. cantonensis. However, the final architecture of the granuloma differed in the two hosts with the cells in the L. rubiginosa granuloma often appearing more vacuolated and less flattened. Nematode development in P. sumatrana was abnormal, with larvae beyond the early first stage occurring in only 21% of infected snails. The highly variable cellular reactions against larvae in P. sumatrana, even within the same snail, probably reflect the differing degrees of maturation attained by individual larvae. Except in one case, no infection of M. tuberculata occurred, presumably as a result of its impenetrable epithelia.     

Parthenites and cercaria of trematodes in the snails Lymnaea saridalensis (Gastropoda, Pulmonata), which inhabits the watershed area of Chany Lake (the South of Western Siberia)

The full list of parthenogenetic larvae and cercaria is presented for the first time for the freshwater snail L. saridalensis (Gastropoda, Pulmonata), which inhabits the watershed area of Chany Lake. It was found that this snail species plays a significant role as the first intermediate host in the life cycles of trematodes in the southern part of Western Siberia. The invasion parameters were calculated for different parasite species. It was found that 50% of the L. saridalensis population serves as the first intermediate host for eleven trematode species that belong to six families: Plagiorchiidae, Echinostomatidae, Diplostomatidae, Strigeidae, Notocotylidae, and Schistosomatidae. The prevalence of infection by each trematoda species in L. saridalensis was determined. Five species of trematodes from the Plagiorchiidae and Echinostomatidae families formed the center of the parasite community, viz., the species Plagiorchis elegans, P. mutationis, Opisthioglyphe ranae, Molinella anceps, and Echinoparyphium aconiatum. Two species, Plagiorchis mutationis and P. multiglandularis, were recorded in the studied area (the Chany Lake watershed area) for the first time at the stages of parthenite and cercaria. It was also found that 1% of L. saridalensis population have multiple (mostly two-species) infections.     

Effects of interspecific competition on asexual proliferation and clonal genetic diversity in larval trematode infections of snails

Interactions among different parasite species within hosts can be important factors shaping the evolution of parasite and host populations. Within snail hosts, antagonistic interactions among trematode species, such as competition and predation, can influence parasite abundance and diversity. In the present study we examined the strength of antagonistic interactions between 2 marine trematodes (Maritrema novaezealandensis and Philophthalmus sp.) in naturally infected Zeacumantus subcarinatus snails. We found approximately the same number of snails harbouring both species as would be expected by chance given the prevalence of each. However, snails infected with only M. novaezealandensis and snails with M. novaezealandensis and Philophthalmus sp. co-occurring were smaller than snails harbouring only Philophthalmus sp. In addition, the number of Philophthalmus sp. rediae was not affected by the presence of M. novaezealandensis sporocysts and the within-host clonal diversity of M. novaezealandensis was not influenced by the presence of Philophthalmus sp. Our results suggest that antagonistic interactions may not be a major force influencing the evolution of these trematodes and that characteristics such as host size and parasite infection longevity are shaping their abundance and population dynamics.     

Clonal diversity driven by parasitism in a freshwater snail

One explanation for the widespread abundance of sexual reproduction is the advantage that genetically diverse sexual lineages have under strong pressure from virulent coevolving parasites. Such parasites are believed to track common asexual host genotypes, resulting in negative frequency‐dependent selection that counterbalances the population growth‐rate advantage of asexuals in comparison with sexuals. In the face of genetically diverse asexual lineages, this advantage of sexual reproduction might be eroded, and instead sexual populations would be replaced by diverse assemblages of clonal lineages. We investigated whether parasite‐mediated selection promotes clonal diversity in 22 natural populations of the freshwater snail Melanoides tuberculata. We found that infection prevalence explains the observed variation in the clonal diversity of M. tuberculata populations, whereas no such relationship was found between infection prevalence and male frequency. Clonal diversity and male frequency were independent of snail population density. Incorporating ecological factors such as presence/absence of fish, habitat geography and habitat type did not improve the predictive power of regression models. Approximately 11% of the clonal snail genotypes were shared among 2–4 populations, creating a web of 17 interconnected populations. Taken together, our study suggests that parasite‐mediated selection coupled with host dispersal ecology promotes clonal diversity. This, in return, may erode the advantage of sexual reproduction in M. tuberculata populations.     

Invasive bivalves increase benthic communities complexity in neotropical reservoirs

Invasive bivalves often act as ecosystem engineers, generally causing physical alterations in the ecosystems in which they establish themselves. However, the effects of these physical alterations over benthic macroinvertebrate communities’ structure are less clear. The objective of this study was to characterize the ecological effects of the invasive bivalves Corbicula fluminea and Limnoperna fortunei on the structure of benthic macroinvertebrate communities in neo-tropical reservoirs. Three hypotheses were tested: (1) invasive bivalves act as facilitator species to other benthic macroinvertebrates, resulting in communities with higher number of species, abundance and diversity; (2) invasive bivalves change the taxonomic composition of benthic macroinvertebrate communities; (3) invasive bivalves increase the complexity of benthic macroinvertebrate communities. For that it was used data from 160 sampling sites from four reservoirs. We sampled sites once in each area, during the dry season from 2009 to 2012. The first hypothesis was rejected, as the presence of invasive bivalves significantly decreased the host benthic communities’ number of species and abundance. The second hypothesis was corroborated, as the composition of other benthic macroinvertebrates was shown to be significantly different between sites with and without invasive bivalves. We observed a shift from communities dominated by common soft substrate taxa, such as Chironomidae and Oligochaeta, to communities dominated by the invasive Gastropoda Melanoides tuberculata. The biomass data corroborated that, showing significantly higher biomass of M. tuberculata in sites with invasive bivalves, but significantly lower biomass of native species. Benthic macroinvertebrate communities presenting invasive bivalves showed significantly higher eco-exergy and specific eco-exergy, which corroborate the third hypothesis. These results suggest that while the presence of invasive bivalves limits the abundance of soft bottom taxa such as Chironomidae and Oligochaeta, it enhances benthic communities’ complexity and provide new energetic pathways to benthic communities in reservoirs. This study also suggests a scenario of invasion meltdown, as M. tuberculata was facilitated by the invasive bivalves.     

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.     

ECOLOGY OF THE INTRODUCED SNAIL MELANOIDES TUBERCULATA (GASTROPODA: THIARIDAE) IN RELATION TO BIOMPHALARIA GLABRATA IN THE MARSHY FOREST ZONE OF GUADELOUPE, FRENCH WEST INDIES

Melanoides tuberculata was introduced to several types of aquatichabitat occurring in the marshy forest zone, Guadeloupe, asa competitor of the snail host, Biomphalaria glabrata, of Schistosomamansoni. Colonization by the competitor was successful in allhabitats, but the impact on the snail host was variable accordingto the site. Evolution of global prevalences, intensities andabundances of Schistosoma mansoni in the reservoir host, Rattusrattus, did not show any significant changes during the eightyears following the introduction of the competitor. The analysisof size distribution of M. tuberculata in a release plot showedthat maximum reproduction took place during the rainy seasonbetween June and November. The thiarid snail needed 4.5 monthsto reach a size of 10 mm, 14 months to reach 15 mm, and morethan 30 months to reach 20 mm. Calculated life expectancieswere 0.74 year at the first year of age, 0.9 year at the secondyear, and 0.5 year at the third year. (Received 21 September 1992; accepted 5 January 1993)     

Invasive Snails and an Emerging Infectious Disease: Results from the First National Survey on Angiostrongylus cantonensis in China

Background

Eosinophilic meningitis (angiostrongyliasis) caused by Angiostrongylus cantonensis is emerging in mainland China. However, the distribution of A. cantonensis and its intermediate host snails, and the role of two invasive snail species in the emergence of angiostrongyliasis, are not well understood.

Methodology/Principal Findings

A national survey pertaining to A. cantonensis was carried out using a grid sampling approach (spatial resolution: 40×40 km). One village per grid cell was randomly selected from a 5% random sample of grid cells located in areas where the presence of the intermediate host snail Pomacea canaliculata had been predicted based on a degree-day model. Potential intermediate hosts of A. cantonensis were collected in the field, restaurants, markets and snail farms, and examined for infection. The infection prevalence among intermediate host snails was estimated, and the prevalence of A. cantonensis within P. canaliculata was displayed on a map, and predicted for non-sampled locations. It was confirmed that P. canaliculata and Achatina fulica were the predominant intermediate hosts of A. cantonensis in China, and these snails were found to be well established in 11 and six provinces, respectively. Infected snails of either species were found in seven provinces, closely matching the endemic area of A. cantonensis. Infected snails were also found in markets and restaurants. Two clusters of A. cantonensis–infected P. canaliculata were predicted in Fujian and Guangxi provinces.

Conclusions/Significance

The first national survey in China revealed a wide distribution of A. cantonensis and two invasive snail species, indicating that a considerable number of people are at risk of angiostrongyliasis. Health education, rigorous food inspection and surveillance are all needed to prevent recurrent angiostrongyliasis outbreaks.     

Differential Parasitism of Native and Introduced Snails: Replacement of a Parasite Fauna

The role of parasites in a marine invasion was assessed by first examining regional patterns of trematode parasitism in the introduced Japanese mud snail, Batillaria cumingi (= B. attramentaria), in nearly all of its introduced range along the Pacific Coast of North America. Only one parasite species, which was itself a non-native species, Cercaria batillariae was recovered. Its prevalence ranged from 3 to 86%. Trematode diversity and prevalence in B. cumingi and a native sympatric mud snail, Cerithidea californica, were also compared in Bolinas Lagoon, California. Prevalence of larval trematodes infecting snails as first intermediate hosts was not significantly different (14% in B. cumingi vs 15% in C. californica). However, while the non-native snail was parasitized only by one introduced trematode species, the native snail was parasitized by 10 native trematode species. Furthermore, only the native, C. californica, was infected as a second intermediate host, by Acanthoparyphium spinulosum(78% prevalence). Given the high host specificity of trematodes for first intermediate hosts, in marshes where B. cumingi is competitively excluding C. californica, 10 or more native trematodes will also become locally extinct.     

Spatial variation in infection by digenetic trematodes in a population of freshwater snails (Potamopyrgus antipodarum)

Larval digenetic trematodes commonly castrate their first intermediate hosts, and should therefore impose strong selection on the timing and mode of host reproduction. Here we examine spatial variation in infection by trematodes in the freshwater snail Potamopyrgus antipodarum. Snails were collected at 11 different sites at Lake Alexandrina on the South Island of New Zealand from transects that ran perpendicular to the shore and across several different habitat types (from 0 to 8 m deep). Logistic regression was used to analyze the relationships between the frequency of trematode infection and snail size, habitat type, and transect location. On average, the probability of infection increased 3.3 times with each 1 mm increase in shell length. Prevalence of infection by the most common species of trematode, Microphallus sp., was highest in the shallow-water habitats where its final hosts (waterflow) spend most of their time. Prevalence of infection by another parasite, Telogaster ophistorchis (final host: eels) increased with depth, but because Microphallus was much more common, total infection by all trematodes decreased with depth. The effects of transect location were minor for Telogaster, but there was significant variation in Microphallus prevalence among transects, especially in the shore-bank habitat. Taken together, these results suggest that the risk of infection is spatially variable, but generally higher in shallow-water habitats, which may explain the greater frequency of sexual individuals as well as earlier reproduction among individuals near shore.     

Invaders of an invader - Trematodes in Potamopyrgus antipodarum in Poland

The subject of the following study was the natural and experimental invasion of trematode larvae in Potamopyrgus antipodarum from Bory Tucholskie National Park (Poland). Only one out of the 14,908 dissected specimens had oval sporocysts and mature cercariae of fish fluke, which belongs to the Sanguinicolidae family. It is the first recorded case in the European population of P. antipodarum living in inland water. The experimental study showed the possibility of native metacercariae (Echinostoma revolutum, Echinoparyphium aconiatum and Hypoderaeum conoideum) settlement in those immigrant snail species; however, exposure to parasites resulted in an increase in snail mortality. The three out of six used cercariae species were able to transform into metacercariae in P. antipodarum as in the second intermediate host, but the exposure to parasitic larvae of four of the used species resulted in an increase in snails’ mortality. It may suggest that not only metacercariae settlement but also the attack of cercariae (Rubenstrema opisthovitellinum at a temperature of 22 °C) affected the low survival of experimental snails in comparison to control animals. The subject of discussion presented in this paper is also the hypothesis on probable effect of the interaction between P. antipodarum and native snail species (as a source of invasive larvae of parasites) living in the same habitat.