Exploring the evolutionary potential of parasites: Larval stages of pathogen digenic trematodes in their thiarid snail host Tarebia granifera in Thailand

Minute intestinal flukes from several distinct families of endoparasitic platyhelminths are a medically important group of foodborne trematodes prevalent throughout Southeast Asia and Australasia. Their lifecycle is complex, with freshwater snails as primary intermediate hosts, with infecting multiple species of arthropods and fish as second intermediate hosts, and with birds and mammals including humans as definitive hosts. In Southeast Asian countries, the diversity of snail species of the Thiaridae which are frequently parasitized by trematode species is extremely high. Here, the thiarid Tarebiagranifera in Thailand was studied for variation of trematode infections, by collecting the snails every two months for one year from each locality during the years 2004–2009, and during 2014–2016 when snails from the same localities were collected and new localities found. From ninety locations a total of 15,076 T.granifera were collected and examined for trematode infections. With 1,577 infected snails the infection rate was found to be 10.46 %. The cercariae were categorized into fifteen species from eight morphologically distinguishable types representing several distinct families, viz. (i) virgulate xiphidiocercariae (Loxogenoidesbicolor, Loxogenesliberum and Acanthatriumhistaense), (ii) armatae xiphidiocercariae cercariae (Maritreminoidescaridinae and M.obstipus); (iii) parapleurophocercous cercariae (Haplorchispumilio, H.taichui and Stictodoratridactyla); (iv) pleurophocercous cercariae (Centrocestusformosanus); (v) megarulous cercariae (Philophthalmusgralli); (vi) furcocercous cercariae (Cardicolaalseae, Alariamustelae and Transversotremalaruei); as well as (vii) echinostome-type cercariae, and (viii) gymnocephalous-type cercariae. In addition, a phylogenetic marker (internal transcribed spacers 2, ITS2) was employed in generic and infrageneric level classifications of these trematodes, using sequences obtained from shed cercariae isolated from T.granifera specimens of the second study period collected in various regions in Thailand. We obtained ITS2 sequences of cercariae from nine species (of seven types): Loxogenoidesbicolor, Loxogenesliberum, Maritreminoidesobstipus, Haplorchistaichui, Stictodoratridactyla, Centrocestusformosanus, Philophthalmusgralli, as well as from one species each of echinostome cercariae and gymnocephalous cercariae. Thus, this analysis combines the parasites’ data on morphology and geographical occurrence with molecular phylogeny, aiming to provide the groundwork for future studies looking into more details of the parasite-snail evolutionary relationships.

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Effects of land use on intermediate snail host fauna, abundance, distribution and cercariae infection rate in Omo-Gibe river basin, Ethiopia

10.21203/rs.2.22079/v1 ◽

2020 ◽

Author(s):

Ketema Deribew ◽

Etana Jaleta ◽

Belayhun Mandefro ◽

Zeleke Mekonnen ◽

Delenasaw Yewhalaw ◽

...

Keyword(s):

Land Use ◽

Land Use Change ◽

Fresh Water ◽

River Basin ◽

Anthropogenic Activities ◽

Freshwater Snail ◽

Snail Host ◽

Snail Species ◽

Intermediate Hosts ◽

Biomphalaria Pfeifferi

Abstract Background: Land use and land cover change significantly affects biodiversity, abundance and distribution of intermediate snail host fauna. In Omo-Gibe river basin the extent of land-use change is high due to anthropogenic activities leading to habitat change of freshwater snail intermediate hosts. Most intermediate snail hosts of human Schistosome parasites belong to two genera, Biomphalaria and Bulinus. In Addition, Lymnea spp. is another important host of Fasciola which causes fasciolasis in domestic animals and human. This study aims to assess the effects of land-use on the distribution and abundance of freshwater snail intermediate hosts and cercariae infection rates of fresh water intermediate snail hosts in Omo-Gibe River basin, Ethiopia.Methods: This study was conducted in Omo-Gibe river basin in 130 sampling sites which include rivers, lakes, dams, stream, wetlands and irrigation ditches. At each site data on land use, anthropogenic activities, freshwater snail abundance and species diversity, and water samples were collected. Snails were collected from each sampling sites using a scoop (20cm x 30cm) with a mesh size of 300µm. Snails were sorted by genus on Enamel pan using forceps and preserved in labeled vials containing 75% ethanol. Live snails collected from the same habitat were sorted carefully and put in clean plastic buckets half filled with water. Afterwards, snails were provided with fresh lettuce leaves and maintained in the laboratory. Snails were then identified morphologically to family, genus and to species level. Each snail was examined for cercaria shedding by placing in a petri dish containing water and exposed to the sun for 2 hours. Cercariae were morphologically identified by microscopy. ArcGIS software of version 10.3.1 was used to map snail distribution and data were analysed using SPSS version-20.Results: The results obtained in this study shows clearly that land use change affect the distribution and abundance of fresh water snails in Omo-Gibe river basin. Fresh water snails were more abundant in farmland and settlement areas. Of the total 2,559 freshwater snails collected from 130 surveyed sites in Omo-Gibe river basin, 1749 (68.34%) belongs to medically important snail species. Biomphalaria spp.914 (35.7%),, Lymnea spp.439 (17.1%),, Physa spp. 343(13.4%) and Bulinus spp 53 (2%)). Sphaeriidae group accounted for 810 (31.6%) of the collected specimens. Biomphalaria pfeifferi was the predominant species of the total snail sampled from lakes, wetlands, rivers and irrigation ditches. Biomphalaria pfeifferi was the most infected snail species by different cercariae. Bulinus globosus and L.natalensis were infected by more than one and same type of cercariae. However, none of B. sudanica and P. acuta specimens was infected by trematode.Conclusions: The results of this study revealed that land use change altered the abundance, distribution and diversity of medically important fresh water snails in the study area. In general medically important freshwater snails which include: Biomphalaria spp, Bulinus spp and Lymnaea spp were collected from lakes, rivers, wetlands, irrigation ditches.. The medically important snail species found infected by cercaria are L. natalensis, B. pfeifferi and B. globosus. Biomphalaria pfefferi was the predominant species and highly infected by cercariae. Higher infection rate was observed in snails collected in Farmland (16.59%) and Grassland (36.6%).

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Broad geographic analyses reveal varying patterns of genetic diversity and host specificity among echinostome trematodes in New Zealand snails

Parasitology ◽

10.1017/s0031182014001279 ◽

2014 ◽

Vol 142 (2) ◽

pp. 406-415 ◽

Cited By ~ 2

Author(s):

DEVON B. KEENEY ◽

JASON PALLADINO ◽

ROBERT POULIN

Keyword(s):

New Zealand ◽

Host Specificity ◽

Snail Host ◽

Snail Species ◽

Intermediate Hosts ◽

Species Complexes ◽

Unidentified Species ◽

Geographic Separation ◽

Host Parasite ◽

Related Parasite

SUMMARYHost specificity is a fundamental component of a parasite's life history. However, accurate assessments of host specificity, and the factors influencing it, can be obscured by parasite cryptic species complexes. We surveyed two congeneric species of intertidal snail intermediate hosts, Zeacumantus subcarinatus and Zeacumantus lutulentus, throughout New Zealand to identify the number of genetically distinct echinostome trematodes infecting them and determine the levels of snail host specificity among echinostomes. Two major echinostome clades were identified: a clade consisting of an unidentified species of the subfamily Himasthlinae and a clade consisting of five species of the genus Acanthoparyphium. All five Acanthoparyphium species were only found in a single snail species, four in Z. subcarinatus and one in Z. lutulentus. In contrast, the Himasthlinae gen. sp. was found in both hosts, but was more prevalent in Z. lutulentus (97 infections) than Z. subcarinatus (10 infections). At least two of the Acanthoparyphium spp. and the Himasthlinae gen. sp. are widespread throughout New Zealand, and can therefore encounter both snail species. Our results suggest that host specificity is determined by host–parasite incompatibilities, not geographic separation, and that it can evolve in different ways in closely related parasite lineages.

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Ecology of larval trematodes in three marine gastropods

Parasitology ◽

10.1017/s0031182002001452 ◽

2002 ◽

Vol 124 (7) ◽

pp. 43-56 ◽

Cited By ~ 28

Author(s):

L. A. CURTIS

Keyword(s):

Snail Host ◽

Trematode Species ◽

Ecological Knowledge ◽

Snail Population ◽

Ilyanassa Obsoleta ◽

Marine Gastropods ◽

Marine Systems ◽

System A ◽

Multiple Species ◽

Host Parasite

To comprehend natural host–parasite systems, ecological knowledge of both hosts and parasites is critical. Here I present a view of marine systems based on the snail Ilyanassa obsoleta and its trematodes. This system is reviewed and two others, those of the snails Cerithidea californica and Littorina littorea, are then summarized and compared. Trematodes can profoundly affect the physiology, behaviour and spatial distribution of hosts. Studying these systems is challenging because trematodes are often embedded in host populations in unappreciated ways. Trematode prevalence is variable, but can be high in populations of all three hosts. Conditions under which single- and multiple-species infections can accumulate are considered. Adaptive relations between species are likely the most important and potentials for adaptation of parasites to hosts, hosts to parasites, and parasites to other parasites are also considered. Even if colonization rate is low, a snail population can develop high trematode prevalence, if infections persist long and the host is long-lived and abundant. Trematodes must be adapted to use their snail hosts. However, both I. obsoleta and L. littorea possess highly dispersed planktonic larvae and trematode prevalence is variable among snail populations. Host adaptation to specific infections, or even to trematodes in general, is unlikely because routine exposure to trematodes is improbable. Crawl-away juveniles of C. californica make adaptation to trematodes in that system a possibility. Trematode species in all three systems are not likely adapted to each other. Multiple-species infections are rare and definitive hosts scatter parasite eggs among snail populations with variable prevalences. Routine co-occurrence of trematodes in snails is thus unlikely. Adaptations of these larval trematodes to inhabit the snail host must, then, be the basis for what happens when they do co-occur.

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Epidemiological and genetic characterization of larval stages of Fasciola gigantica in snail intermediate hosts in Karnataka State, India

Acta Parasitologica ◽

10.1515/ap-2018-0070 ◽

2018 ◽

Vol 63 (3) ◽

pp. 609-616

Author(s):

Rangappa Rajanna ◽

Pamalapati Mahadevareddy Thimmareddy ◽

Pinaki Prasad Sengupta ◽

Susan Jacob Siju ◽

Gotakanapura Sanjeevamurthy Mamatha

Keyword(s):

Western Ghats ◽

Coastal Region ◽

Fasciola Gigantica ◽

Internal Transcribed Spacers ◽

Nuclear Ribosomal Dna ◽

Intermediate Hosts ◽

Nested Polymerase Chain Reaction ◽

Larval Stages ◽

Geographical Regions ◽

Deccan Plateau

Abstract Fasciolosis in ruminants in India is caused by the liver fluke Fasciola gigantica. Radix (Lymnaea) spp. are known to carry the infective stages of this parasite. Understanding the seasonal prevalence of F. gigantica infection in the intermediate host is of extreme importance in order to elucidate the transmission dynamics of the parasite. So the present study was designed to determine the bioclimatic distribution of larval stages of F. gigantica in Radix spp. snails as well as to explore the genetic diversity of F. gigantica in three geographical regions (Deccan plateau, Western Ghats and coastal region) of Karnataka. The lymnaeid snails were sampled (n = 2077) for a period of one year (June 2015 to May 2016) at 24 sites. The snails were morphologically identified and the infection status was established through cercarial shedding and nested polymerase chain reaction (PCR) based technique targeting second internal transcribed spacers (ITS-2) of nuclear ribosomal DNA. The sensitivity of PCR (8.2%) for detection of F. gigantica infection within snail is significantly higher than cercarial shedding (4.3%) with an overall prevalence of 5.1%. The prevalence of infection was higher in winter than in the rainy and summer seasons (6.2% instead of 4.6% and 4.3% respectively). Deccan plateau (5.8%) showed a higher prevalence of infection compared to Western Ghats (5.2%) and Coastal region (3.6%). The sequencing ITS-2 region permitted the identification of the parasite as F. gigantica which is having high implication in studying the population genetic structure of the parasite in the country. In conclusion, overall results indicated that Radix spp. snails harboured F. gigantica developmental stages throughout the year and nested PCR was found to be sensitive and specific for detection of F. gigantica infection in snails compared to routine parasitological techniques.

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The life cycle and transmission dynamics of the larval stages ofHypoderaeum conoideum

Journal of Helminthology ◽

10.1017/s0022149x00000238 ◽

2000 ◽

Vol 74 (2) ◽

pp. 165-172 ◽

Cited By ~ 9

Author(s):

C. Muñoz-Antolí ◽

R. Toledo ◽

J.G. Esteban

Keyword(s):

Life Cycle ◽

Freshwater Snail ◽

Transmission Dynamics ◽

Freshwater Snails ◽

Snail Species ◽

Intermediate Hosts ◽

Free Living ◽

Larval Stages ◽

Life History Stages ◽

First Intermediate Host

AbstractThe morphology of the different larval stages and life cycle ofHypoderaeum conoideum(Trematoda: Echinostomatidae) are described. The freshwater snail speciesLymnaea peregra(Gastropoda: Lymnaeidae) serves as the natural first intermediate host and this andL. corvusserve as experimental first intermediate hosts. These and other freshwater snails, such asPhysella acutaandGyraulus chinensis, in turn serve as second intermediate hosts. Adult worms were obtained from chicks and ducks, but not from rats, mice and golden hamsters. The morphology of the larval stages is compared with previous work onH. conoideum. Several aspects of the biology of the life history stages are described with emphasis on the transmission dynamics of the free-living stages. Differential suitability of the snail species that may act as first and/or second intermediate hosts is studied and discussed.

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Exposing the Barcoding Void: An Integrative Approach to Study Snail-Borne Parasites in a One Health Context

Frontiers in Veterinary Science ◽

10.3389/fvets.2020.605280 ◽

2020 ◽

Vol 7 ◽

Author(s):

Ruben Schols ◽

Aspire Mudavanhu ◽

Hans Carolus ◽

Cyril Hammoud ◽

Kudzai C. Muzarabani ◽

...

Keyword(s):

One Health ◽

Parasite Species ◽

Integrative Approach ◽

Trematode Species ◽

Nuclear Rdna ◽

Closely Related Species ◽

Larval Stages ◽

Coi Barcoding ◽

Reference Sequences ◽

Trematode Infections

Trematodes are snail-borne parasites of major zoonotic importance that infect millions of people and animals worldwide and frequently hybridize with closely related species. Therefore, it is desirable to study trematodiases in a One Health framework, where human and animal trematodes are considered equally important. It is within this framework that we set out to study the snail and trematode communities in four artificial lakes and an abattoir in Zimbabwe. Trematode infections in snails were detected through multiplex PCR protocols. Subsequently, we identified snails by sequencing a partial mitochondrial cytochrome c oxidase subunit I (COI) fragment, and trematodes (adults from the abattoir and larval stages detected in snails) using COI and nuclear rDNA markers. Of the 1,674 collected snails, 699 were molecularly analyzed, in which we identified 12 snail and 19 trematode species. Additionally, three parasite species were sampled from the abattoir. Merely four trematode species were identified to species level through COI-based barcoding. Moreover, identification of members of the superfamilies Opisthorchioidea and Plagiorchioidea required a phylogenetic inference using the highly conserved 18S rDNA marker, as no related COI reference sequences were present in public databases. These barcoding challenges demonstrate a severe barcoding void in the available databases, which can be attributed to the neglected status of trematodiases. Adding to this, many available sequences cannot be used as different studies use different markers. To fill this gap, more studies on African trematodes, using a standardized COI barcoding region, are desperately needed.

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Tranmission pattern differences of miracidia and cercariae larval stages of digenetic trematode parasites

Acta Parasitologica ◽

10.1515/ap-2016-0095 ◽

2016 ◽

Vol 61 (4) ◽

Cited By ~ 4

Author(s):

Michael R. Zimmermann ◽

Kyle E. Luth ◽

Gerald W. Esch

Keyword(s):

Abiotic Factors ◽

Field Studies ◽

Life Cycles ◽

Digenetic Trematode ◽

Snail Species ◽

Intermediate Hosts ◽

Complex Life Cycles ◽

Larval Stages ◽

Digenetic Trematodes ◽

Trematode Parasites

AbstractDigenetic trematodes have complex life cycles involving multiple hosts and free-living larval stages. Some species have 2 lar-val stages that infect snails, with miracidia and cercariae using these molluscs as first and second intermediate hosts, respec-tively. Although both larval stages may infect the same snail species, this is accomplished using different chemical cues and may be influenced by different biotic and abiotic factors. Significant differences in the infection patterns of these parasitic stages regarding host size and density were observed in 2 separate field studies. The prevalence of sporocysts/rediae and mean abundance of

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Molecular and morphological characterization of the cercariae of Lecithodendrium linstowi (Dollfus, 1931), a trematode of bats, and incrimination of the first intermediate snail host, Radix balthica

Parasitology ◽

10.1017/s0031182017001640 ◽

2017 ◽

Vol 145 (3) ◽

pp. 307-312 ◽

Cited By ~ 2

Author(s):

EGIE E. ENABULELE ◽

SCOTT P. LAWTON ◽

ANTHONY J. WALKER ◽

RUTH S. KIRK

Keyword(s):

Intermediate Host ◽

Molecular Data ◽

Morphological Characterization ◽

Snail Host ◽

Intermediate Hosts ◽

Larval Stages ◽

Life Cycle Stages ◽

Radix Balthica ◽

First Intermediate Host

SUMMARYLecithodendrium linstowi is one of the most prevalent and abundant trematodes of bats, but the larval stages and intermediate hosts have not been identified. We present the first molecular and morphological characterization of the cercariae of L. linstowi based on a phylogenetic analysis of partial fragments of LSU and ITS2 rDNA. The first intermediate host was incriminated as Radix balthica by DNA barcoding using cox1 and ITS2 sequences, although the snail morphologically resembled Radix peregra, emphasizing the requirement for molecular identification of lymnaeids as important intermediate hosts of medical and veterinary impact. The application of molecular data in this study has enabled linkage of life cycle stages and accurate incrimination of the first intermediate host.

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Infection patterns of trematodes across size classes of an invasive snail species using field and laboratory studies

Parasitology ◽

10.1017/s0031182018001646 ◽

2018 ◽

Vol 146 (4) ◽

pp. 438-444 ◽

Cited By ~ 1

Author(s):

Rebecca Z. Bachtel ◽

Matthew Rittenhouse ◽

Gregory J. Sandland ◽

Jennifer A. H. Koop

Keyword(s):

Host Population ◽

Snail Host ◽

Host Susceptibility ◽

Snail Species ◽

Infection Prevalence ◽

Laboratory Studies ◽

Intermediate Hosts ◽

Susceptible Host ◽

Transmission Potential ◽

River Region

AbstractIn the Upper Mississippi River Region, invasive faucet snails (Bithynia tentaculata) and their trematode parasites have been implicated in more than 182 000 waterfowl deaths since 1996. Estimating transmission potential depends on accurate assessments of susceptible host population size. However, little is known about the mechanisms underlying snail–host susceptibility in this system. Prior field studies suggest that very small, likely young, faucet snails are less suitable secondary intermediate hosts. Here, we test whether the patterns observed in the field are because small snails (1) are refractory to infection by cercariae, (2) die from infection and are removed from sampled populations, and/or (3) are not preferred by cercariae. Our own field collections were consistent with the observation that smaller faucet snails exhibit lower metacercarial infection prevalence and abundance than larger snails. However, laboratory-based experiments show that smaller snails were actually more susceptible to infection than larger snails. Moreover, the smallest snail size class had significantly higher mortality than larger snails following infection, which may explain their reduced infection levels observed in the field. Our study demonstrates the importance of pairing field and laboratory studies to better understand mechanisms underlying patterns of infection.

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Global warming and temperature-mediated increases in cercarial emergence in trematode parasites

Parasitology ◽

10.1017/s0031182005008693 ◽

2005 ◽

Vol 132 (1) ◽

pp. 143-151 ◽

Cited By ~ 237

Author(s):

R. POULIN

Keyword(s):

Global Warming ◽

Geographical Distribution ◽

Climate Models ◽

Extreme Values ◽

Geometric Mean ◽

Effect Of Temperature ◽

Trematode Species ◽

Intermediate Hosts ◽

Cercarial Production ◽

Trematode Parasites

Global warming can affect the world's biota and the functioning of ecosystems in many indirect ways. Recent evidence indicates that climate change can alter the geographical distribution of parasitic diseases, with potentially drastic consequences for their hosts. It is also possible that warmer conditions could promote the transmission of parasites and raise their local abundance. Here I have compiled experimental data on the effect of temperature on the emergence of infective stages (cercariae) of trematode parasites from their snail intermediate hosts. Temperature-mediated changes in cercarial output varied widely among trematode species, from small reductions to 200-fold increases in response to a 10 °C rise in temperature, with a geometric mean suggesting an almost 8-fold increase. Overall, the observed temperature-mediated increases in cercarial output are much more substantial than those expected from basic physiological processes, for which 2- to 3-fold increases are normally seen. Some of the most extreme increases in cercarial output may be artefacts of the methods used in the original studies; however, exclusion of these extreme values has little impact on the preceding conclusion. Across both species values and phylogenetically independent contrasts, neither the magnitude of the initial cercarial output nor the shell size of the snail host correlated with the relative increase in cercarial production mediated by rising temperature. In contrast, the latitude from which the snail-trematode association originated correlated negatively with temperature-mediated increases in cercarial production: within the 20 ° to 55 ° latitude range, trematodes from lower latitudes showed more pronounced temperature-driven increases in cercarial output than those from higher latitudes. These results suggest that the small increases in air and water temperature forecast by many climate models will not only influence the geographical distribution of some diseases, but may also promote the proliferation of their infective stages in many ecosystems.

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