Schistosomes in the Persian Gulf: novel molecular data, host associations, and life-cycle elucidations | Scientific Reports – Nature.com

Schistosomes in the Persian Gulf: novel molecular data, host associations, and life-cycle elucidations | Scientific Reports – Nature.com

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.
Advertisement
Scientific Reports volume 12, Article number: 13461 (2022)
Metrics details
Avian schistosomes, comprise a diverse and widespread group of trematodes known for their surprising ability to switch into new hosts and habitats. Despite the considerable research attention on avian schistosomes as causatives of the human cercarial dermatitis, less it is known about the diversity, geographical range and host associations of the marine representatives. Our molecular analyses inferred from cox1 and 28S DNA sequence data revealed presence of two schistosome species, Ornithobilharzia canaliculata (Rudolphi, 1819) Odhner, 1912 and a putative new species of Austrobilharzia Johnston, 1917. Molecular elucidation of the life-cycle of O. canaliculata was achieved for the first time via matching novel and published sequence data from adult and larval stages. This is the first record of Ornithobilharzia from the Persian Gulf and globally the first record of this genus in a potamidid snail host. Our study provides: (i) new host and distribution records for major etiological agents of cercarial dermatitis and contributes important information on host-parasite relationships; (ii) highlights the importance of the molecular systematics in the assessment of schistosome diversity; and (iii) calls for further surveys to reach a better understanding of the schistosome diversity and patterns of relationships among them, host associations, transmission strategies and distribution coverage.
Avian schistosomes comprise a diverse and widespread group known for their surprising ability to switch into new hosts and habitats1. Their cercariae are recognised as important causative agents of the waterborne allergic disease cercarial dermatitis (2 and references therein). However, the current systematics and taxonomy of the group is exclusively based on morphological characters of the adults. Difficulties in the identification of their larval stages and the lack of suitability of experimental approaches in large-scale screening studies of natural infections in intermediate hosts, has hindered the real assessment of their diversity, host and distributional ranges3. Often larval and adult stages from natural infections in snails and birds have been assigned to belong to the same species with the lack of further evidence linking their conspecificity. The discovery of avian schistosome diversity, their life-cycle elucidations and taxonomy has largely benefited from molecular phylogenetics studies (2,4 and references therein). To date, a total of 13 genera of avian schistosomes with about 70 species and 20 species-level genetically distinct lineages are known around the globe4,5. Based on the habitat where their life-cycles take place, avian schistosomes consist of freshwater and marine representatives.
Marine schistosomes represent a small group of widely distributed digeneans that are parasitic as adults in the vascular systems of various birds6. A predominant part of the extant marine schistosomes is known to parasitise charadriiforms (gulls and/or terns) with a few records in spheniscids5,6. Currently, four genera, Austrobilharzia Johnston, 1917, Gigantobilharzia Odhner, 1910, Marinabilharzia Lorenti, Brant, Gilardoni, Díaz & Cremonte, 2022 and Ornithobilharzia Odhner, 1912 are known to have marine-based life-cycles4,5. Of these, Ornithobilharzia Odhner, 1912 and Austrobilharzia Johnston, 1917 were recognised as an earlier diverging group which gave rise to all existent schistosomes7. Although, schistosomes represent a well-circumscribed monophyletic group, monophyly for the avian representatives has been rejected4,7. Phylogenetic hypotheses, revealed a basal switch from marine to freshwater environment which has occurred along a switch from caenogastropod to heterobranch snails1. A secondary switch from freshwater to marine environments has been suggested to have occurred with colonisation of heterobranch snails from the families Haminoeidae Pilsbry, 1895 and Siphonariidae Gray, 18278,9,10.
Ornithobilharzia canaliculata was first described by Rudolphi (1819) as Distoma canaliculatum, the first schistosome species reported from the intestine of terns (“Sternae species brasilianae”) in Brazil11. In 1912, Odhner12 erected the genus Ornithobilharzia and defined D. canaliculatum as the type-species. Despite the wide range of known definitive hosts including marine birds of six genera (Larus L., Sterna L., Chlidonias Rafinesque, Hydroprogne Kaup, Puffinus (Manxsherwater), and Thalasseus F. Boie), and a wide geographical range across the Holarctic and Neotropics13, only a single marine gastropod species, Lampanella minima (Gmelin), has been assigned as the intermediate host in the Gulf of Mexico14. However, experimental elucidation of the life-cycle has never been carried out and a formal description of the cercaria of O. canaliculata is still lacking. Under the current taxonomic treatment, the genus includes three species: O. amplitesta Gubanov & Mamaev in Mamaev, 1959; O. canaliculata (Rudolphi, 1819) Odhner, 1912; and O. lari McLeod, 1937.
The closely-related genus Austrobilharzia Johnston, 1917 currently comprises 4 species: A. odhneri (Faust, 1924) Farely, 1971; A. penneri Short & Holliman, 1961; A. terrigalensis Johnston, 1917; and A. variglandis (Miller & Northup, 1926) Penner 1953. The genus was erected by Johnston (1917) to accommodate A. terrigalensis, a species found in the intestine of Larus novae-hollandiae shot at Terrigal, New South Wales, Australia. Caenogastropod snails have been reported as the natural intermediate hosts15,16,17,18. However, a combination of identification and taxonomic problems, have led to the biological paradox of a single species, A. terrigalensis, occurring at three distinct geographical regions and utilising different species of caenogastropod and bird hosts. Based on the geographical distribution, A. terrigalensis was assumed to occur in Larus novae-hollandiae and Batillaria australis in Australia; A. valisineria, Mergus serrator L., Aythya affinis Eyton, 1838 and Ilyanassa obsoleta (Say) in North America; and Arenaria interpres (L.) and Littorina pintado (W. Wood, 1828) in the Pacific.
Caenogastropods are one of the most diverse groups of gastropods comprising about 60% of the known species with predominantly marine forms19 and are known as intermediate hosts for a variety of trematode parasites15,20,21. Members of the genus Pirenella J. E. Gray are abundant inhabitants of intertidal sedimentary shores with wide geographical distribution ranging from the western Pacific and Indian Ocean to the eastern Mediterranean Sea. A recent study reported a total of 16 valid species within the genus, with some species known as inhabitants of extreme environments, from brackish estuaries to hypersaline lagoons and inland lakes22. Pirenella cingulata (Gmelin, 1791) is the most abundant caenogastropod species in the Persian and Oman Gulfs. It is known for its tolerance to environmental extremes and ability to flourish in intertidal muddy or sandy substrates, as well as mudflats adjacent to mangrove forests23,24.
As part of an ongoing study aiming to characterise trematode diversity in the horn snail (Pirenella cingulata) along the coast of Iran, we here report on the diversity of avian schistosomes associated with marine life-cycles using cox1 and 28S rDNA sequence data. The present study is the first to molecularly elucidate the life-cycle of the first ever described schistosome, O. canaliculata, and further reports on a putative new species of Austrobilharzia. Both species recovered are of the largely understudied marine schistosomes known for their implication as causative agents of cercarial dermatitis. This is the first unambiguous documentation that the potamidid snail P. cingulata is the natural snail host for O. canaliculata. The evolutionary relationships and host-parasite associations among the avian schistosomes are further revisited.
Three out of the 1,745 examined P. cingulata were infected with avian schistosomes. The infected snails were collected at two distinct localities named Genaveh (n = 2; prevalence = 1%) and Jask (n = 1; prevalence = 0.4%) (see also Fig. 1 for sampling locations). Successful amplifications were achieved for 28S and cox1 for all three isolates. The yielded sequences were 1254–1285 bp (28S rDNA) and 344–730 bp long (cox1). The two isolates from Genaveh shared an identical 28S rDNA sequence with a published isolates for Ornithobilharzia canaliculata from the USA ex Larus delawarensis and L. occidentalis (AF167085, AY157248, KP734309), while the isolate from Jask differed by 2.3% (29 bp) from the former ones. A BLASTn search indicated that the latter isolate belonged to the genus Austrobilharzia. The novel isolate from Iran differed by 12–19 bp (0.9–1.8%) from the published representatives of the genus. The closest relative was an otherwise unidentified isolate from the same host species, P. cingulata, from off Kuwait (12 bp, 0.9% genetic difference).
(A) General view map, generated using QGIS version 3.4 (http://www.qgis.org)52, and (B) sampling localities along the Persian Gulf and the Gulf of Oman off Iran. Points correspond to the sampling localities. Abbreviations: A, Azini; D, Dargahan; G, Genaveh; J, Jask; M, Geshm; S, Shif; T, Bandar Abbas; Y, Deylam; U, Bushehr. (C) Snail intermediate host Pirenella cingulata (Gmelin, 1791). (D) Cercaria collected from P. cingulata. Scale-bar = 100 µm.
Cox1 sequence divergence between our two isolates of O. canaliculata from Iran was 9 bp (2.6%). In contrast to the identical 28S sequences between the novel and published isolates for O. canaliculata, cox1 sequences differed substantially, ranging between 27 and 32 bp (7.9–9.3%). The single isolate from Jask differed by 1.66–1.82% (49–55 bp; 16.3–18.2%) from the novel isolates for O. canaliculata, and by 59 bp (20.1%) from Austrobilharizia sp. from Kuwait. Interspecific sequence divergence within Austrobilharzia was within the range of 21–63 bp (9.7–20.1%). However, the intergeneric divergence between the isolates for Ornithobilharzia and Austrobilharzia was somehow lower that the interspecific divergence for Austrobilharzia, i.e., 25–61 bp (7.7–18.4%). A single cox1 isolate for Austrobilharzia variglandis ex Larus sp. from Canada was not included in the sequence comparisons as it covers a distinct region of the cox1 gene and did not align with the remaining published isolates.
The aligned 28S dataset consisted of 76 terminals (2 newly-sequenced) and it was 1370 bp long, 78 of which were excluded prior to analyses. The cox1 dataset comprised 66 terminals and it was 1031 bp long. Analyses of the individual genes resulted in well-resolved trees (Fig. 2). The 28S rDNA hypothesis, presented in Fig. 2A, included representatives of all named and molecularly characterised species-level lineages except for the monotypic Jilinobilharzia as molecular data currently do not exist (the single species, J. crecci Liu & Bai, 1976, has not been reported since its original description). Therefore, the ingroup taxa consisted of representative sequences of the families Schistosomatidae and the closely related Spirorchiidae (see Supplementary Table S1). The outgroup comprised representative of the Aporocotylidae and it was informed from previous phylogenies25. Our phylogenetic hypothesis recovered the spirorchiids in freshwater crocodilian and testudine hosts as the earliest diverging lineage. Spirorchiids with marine life-cycle clustered in a distinct clade basal to the Schistosomatidae. Members parasitic in marine testudines were identified as a distinct clade sister to all remaining schistosomes parasitic in birds and mammals. Schistosomes clustered into four distinct lineages: (i) an earlier diverging and strongly supported clade comprising the marine Ornithobilharzia and Austrobilharzia (ii) Macrobilharzia—a genus known from suliform birds which was resolved as a distinct lineage basal to the freshwater schistosomes, and two strongly-supported multi-taxa sister clades predominantly of (iii) mammalian and (iv) avian schistosomes. The mammalian schistosomes were further recovered as three distinct lineages: (i) Bivitelobilharzia—a genus including species parasitic in elephants and rhinoceros were recovered in a strongly-supported sub-clade sister to the main clade of mammalian schistosomes; (ii) a sub-clade of Schistosoma spp. with South East Asian distribution; and (iii) a clade comprising African representatives of Schistosoma. The North American mammalian representatives, Heterobilharzia and Schistosomatium were resolved as closer relatives to the large clade of avian schistosomes (Trichobilharzia + Marinabilharzia + Dendritobilharzia + Gigantobilharzia + Nasusbilharzia + Riverabilharzia). The remaining avian schistosomes clustered in two sister monophyletic clades with generally strong support for the major nodes. Bilharziella and Nasusbilharzia were recovered as earlier diverging to the two sister strongly-supported subclades of Gigantobilharzia + Dendritobilharzia + Marinabilharzia + Riverabilharzia, and Trichobilharzia + Allobilharzia + Anserobilharzia.
Bayesian analyses of the (A) 28S rDNA and (B) cox1 datasets constructed using MrBayes v. 3.2.3 under the GTR + I + Г model of sequence evolution. Analyses were run for 10,000,000 generation and 25% discarded as “burn-in”. Posterior probability values are given above the branches; values. Nodes with < 0.95 posterior probability support have been collapsed. Branch length scale-bar indicates number of substitutions per site. Newly-generated sequences are indicated in colour indicated red and bold. Hosts of origin of individual sequences are indicated after the specimen’s host name. Branches in blue indicate schistosomes with marine life-cycle. Shaded areas and taxa outlined with doted lines reflect on the current taxonomic framework of the family and also given on the right.
The cox1 tree was well-resolved and received strong support for most of the internal nodes (Fig. 2B). Taxa largely grouped in consistence with the 28S solution. Ornithobilharzia and Austrobbilharzia clustered into two distinct strongly-supported sister clades. The newly-sequenced isolate from Jask clustered in a clade with A. variglandis and A. terrigalensis; however, the isolate for O. canaliculata clustered with otherwise unidentified isolate labelled as Austrobilharzia sp. from Kuwait indicating a possible misidentification of the latter one. This was further confirmed by the high levels of genetic divergence in comparison with the other isolates of Austrobilharzia as indicated above.
The present study is part of an effort to document the trematode diversity in P. cingulata (Gmelin, 1791), one of the most abundant snail species along the Iranian coast23,24,26. Sequence data for two species of marine avian schistosomes, Ornithobilharzia canaliculata (Rudolphi, 1819) and a putative new species of Austrobilharzia Johnston, 1917, are represented in a phylogenetic context together with other members of the family Schistosomatidae. This is the first report and molecular evidence for Ornithobilharzia canaliculata (Rudolphi, 1819) infecting P. cingulata as an intermediate host and it is the first partial molecular elucidation of its life-cycle. Our study adds to the diversity, host associations and phylogeny of the avian schistosomes with marine-based life-cycles, a group of schistosomes with great etiological importance.
Cercariae of the marine schistosomes are recognised as important etiological agents of human dermatitis27,28,29. Despite their importance to the public health, still very little is known about their diversity and evolution7 as a consequence of largely under surveyed marine habitats for schistosomes worldwide4. This is in sharp contrast with the wealth of knowledge gathered about the mammalian and avian schistosomes with freshwater-based life-cycles, and information concerning the natural history of most marine schistosomes is scarce. The slow rates in recovering marine schistosomes, low species richness recorded in snail hosts and the convoluted taxonomy of the group, including separate taxonomic treatments of the distinct life-cycle stages, reflects the scarcity of data30. Matching sequence data for different life-cycle stages and across distant localities has accelerated life-cycles elucidations and host-parasite associations4,5. Although, the molecular systematics has had a major impact for the recent increase in discoveries and species delimitation, it has led to a plethora of putative new species and lineages of avian schistosomes for which only molecular data for their cercarial stages exist. Most of these putative species/species level lineages are of considerable importance due to their etiological significance. Their formal descriptions await as reliably identified adult stages are needed to help infer on their respective life- cycles and host-parasite associations.
Ornithobilharizia canalicata was originally described from Sterna galericulata in Brazil11. Later the species was reported from a wide range of gulls and terns across the Americas, Europe, Asia and New Zealand (see Table 1 for details). Larus dominicanus Lichtenstein and L. maculipennis Lichtenstein serve as the main hosts in the southern hemisphere; Larus delawarensis Ord, and L. occidentalis Audubon have been reported as hosts in North America and a total of 22 species of gulls and terns were reported as hosts across Europe and the Middle East. Despite the large number of definitive hosts, thus far the species was reported only from a single mollusc species, Lampanella minima (Gmelin), in North America. However, an experimental infection linking larval and adult stages has never been conducted. An important result from our study is the molecular confirmation of the conspecificity of our isolate from P. cingulata with the published isolate of an adult worm from North America. Matching sequence data for isolates from different life-cycle stages collected from disparate locations and times, provides unambiguous link between adult and larval stages from natural infections and accelerates species circumscription. The intercontinental distribution and the rather narrowly defined clade of gulls is instructive for studies on the transmission of avian zoonoses and the epidemiology of human cercarial dermatitis. The trans-continental distribution of Ornithobilharzia across the America, Europe and Asia is an explicit example that species dispersal is determined by the most vagile, bird host, involved in the trematode life-cycle. It is widely accepted that the distribution of the definitive host governs the larval trematode recruitment in the snail (first) intermediate host (31 and references therein). Resolving the relative roles of both host ecology and phylogeny in respect to the parasite transmission dynamics over evolutionary times would require further concerted efforts. Phylogenetic studies based on denser and wide taxon sampling including diverse intermediate and definitive hosts is crucial for building up an improved framework and better interpretation of the schistosome biology3. Further, good documentation and re-evaluation of the morphological charters of the respective larval stages is urgently needed.
Successful transmission of parasites with complex life-cycles requires an overlap of all hosts involved. The invertebrate first intermediate host has been recognised as one of the keys to the evolutionary expansions of the digenean trematodes. All schistosomes (marine and freshwater) are known to develop in gastropods. The basal position of the marine schistosomes (Austrobilharzia and Ornithobilharzia) has been considered as an indication for a successful ancestral marine-transmitted bird parasite transmission in colonising both freshwater snails and mammals25. The schistosomes emerging from marine heterobranch snails (Haminea and Siphonaria) and also recorded in penguins are a well-known example of secondary colonisation of marine habitats by the schistosomes30,32,33. Considering the snail intermediate hosts, in at least two instances, even congeneric schistosomes depend on markedly divergent gastropod lineages, i.e., pulmonates versus opisthobranchs or caenogastropods, indicative for an extensive host switching within the molluscan hosts34 and references therein).
Avian schistosomes are known to have colonized a wide range of snail hosts with representatives from 15 snail families: (i) caenogastropods from both marine (Potamididae, Batilariidae, Nassariidae, and Littorinidae14,15,35,36,37 and freshwater environments (Thiaridae, Ampullariidae, Hydrobiidae, and Semisulcospiridae35,38,39,40,41; (ii) heterobranchs from marine (Haminoeidae8,9, and freshwater (Valvatidae42; and (iii) pulmonates from marine (Siphonariidae10) and freshwater (Physidae, Lymnnaeidae, Planorbidae, and Chilinidae1,3,35,43,44. Reports of avian schistosomes from distantly related snail intermediate hosts are not rare and invoke questions on the proper identification of the respective parasites. Dendritobilharzia pulverulenta45 Skrjabin, 1924 has been reported from two distinct planorbid snails Gyraulus Charpentier, 1837 and Anisus vortex (L.)46. Gyraulus has been reported as a natural host of the species in North America and New Zealand, while Anisus and Planorbis planorbis (L.) have been reported as hosts in Europe. Trichobilharzia jequitibaensis Leite, Costa, & Costa, 1978 is known to infect both lymnaeid and physid snails47. Austrobilharzia terrigalensis has been considered to utilise distinct snail hosts across its distributional range in Australia (Batillaria australis (Quoy & Gaimard)), North America (Cerithideopsis scalariformis (Say), and Ilyanassa obsoleta (Say) and the Pacific (Littorina pintado (W. Wood)). Intercontinental and trans-hemispheric distribution has been recently reported for Trichobilharzia querquedule48,49, however the species is known as a parasite specific to Physa spp. as an intermediate host.
In respect to their definitive hosts, a predominant part of the schistosomes is known as parasitises in birds. Currently a total of 13 genera are known as parasites in birds: Austrobilharzia Johnston, 1917 (6 species), Allobilharzia (1 species), Anserobilharzia (1 species), Bilharziella (1 species), Dendritobilharzia (2 species) Gigantobilharzia (c.14 species), Jilinobilharzia (1 species), Macrobilharzia Travassos, 1922 (2 species), Ornithobilharzia Odhner, 1912 (3 species); Nasusbilharzia Flores50 (1 species), Marinabilharzia (1 species), Riverabilharzia (1 species)5 and Trihobilharzia (c.35 species). Among them, species of Trihobilharzia have been subject of the most intensive research due to their recognition as leading etiological agents of human cercarial dermatitis (51 and references therein). The genus represents the most speciose among the bird schistosomes with about 35 species or species level lineages. However, about 65% of the remaining avian schistosomes, yet remain largely unstudied with fragmentary data on their diversity, biology and ecology. This is especially true in respect to the marine schistosomes for which life-cycle information lags behind their freshwater relatives. Despite the great efforts made so far in building up a comprehensive framework for the study of schistosome diversity, still considerable data are needed for assessing their true diversity due to the difficulty of directly relating larval and adult stages. Consistent efforts towards the use of integrative approach including collecting novel data from diverse host species and combining them thorough morphological examination, traditional systematics, classical taxonomy and phylogenetics have been proven as most valuable practice providing important information to the better understanding of the biodiversity and evolutionary relationships of the group2,3,4.
Our study strongly suggests that the biodiversity of the marine schistosomes is underestimated. The extensive discovery-based studies about schistosome diversity during the last two decades has revealed an immense diversity of avian schistosomes. However, unravelling their true diversity across hosts and geographic areas have been hindered by the difficulties of matching distinct life-cycle stages. There is still a need for more records of identifiable adult and larval schistosomes. Our study is a crucial step towards better understanding of important properties of marine schistosome biology and ecology, their patterns of diversification and distribution.
A total of 1745 adult P. cingulata (Gmelin, 1791) were sampled from 9 distinct locations along the Iranian coastline between December 2019 and February 2020 (Fig. 1). Samples comprised a minimum of 200 individual snails per locality, which were opportunistically collected by hand at the low tide from the intertidal zone. Snails were transferred alive to the laboratory, where they were measured (length and weigh) and labelled with a unique code given to each specimen. Each snail was then placed in an individual 50 ml beaker filled with filtered seawater and exposed to a warm light source for 3–4 h to simulate cercarial emergence. Beakers were screened under a stereomicroscope for the presence of cercariae indicating patent infections in the snail host. Prepatent infections were detected with snail dissections, which were conducted on the 3rd day of light stimulation. Both the released cercariae and schistosome sporocysts recovered from the host’s tissue were washed with distilled water and preserved in molecular grade ethanol for DNA isolation and sequencing.
Ethanol-preserved samples of pooled cercariae were subjected to DNA extraction and sequencing. Partial cox1 and 28S rDNA sequences were generated for the schistosome parasites recovered in order to achieve molecular identification and carry out reconstruction of their evolutionary relationships using published primers (28S (digl2 + 1500R53,54; ECD2 + 900F55,56 as internal sequencing primers; cox1: JB3 + JB4.557 or CO1-R58). Contiguous sequences were aligned with MAFFT v.759,60 as an online execution. After alignment, sequences for cox1 were checked for stop codons using the echinoderm and flatworm mitochondrial code (translation table 961). All sequences were trimmed in order the first base to correspond to the first codon position in order to simplify position-coding in the downstream analyses.
Phylogenetic analyses were performed on individual gene datasets using Bayesian inference (see Supplementary Table 1 for details on the taxa included in the analyses). Prior to analyses, the ‘best-fitting’ models of nucleotide substitution were estimated based on the Bayesian information criterion (BIC) in jModelTest v. 2.1.462. BI analysis was carried out with MrBayes v. 3.2.763 on the CIPRES Science Gateway v.3.364 using Markov chain Monte Carlo (MCMC) searches on two simultaneous runs of four chains for 107 generations, sampling trees every 103 generations. The “burn-in” determined by stationarity of lnL assessed with Tracer v.1.565 was set for the first 25% of the trees sampled, and a consensus topology and nodal support estimated as posterior probability values66 were calculated from the remaining trees. Phylogenetic trees were visualized and finalised in FigTree v. 1.4.467. The newly-generated sequences were deposited in GenBank under accession numbers: ON928982–ON928984 (cox1), ON938179–ON938181 (28S) in the case of avian schistosomes, and ON911910 (cox1), ON911912 (28S)—for the snail host.
All data are available in the main manuscript or additional supporting files.
Brant, S. V. & Loker, E. S. Molecular systematics of the avian schistosome genus Trichobilharzia (Trematoda: Schistosomatidae) in North America. J. Parasitol. 95, 941–963 (2009).
CAS  PubMed  Article  Google Scholar 
Horák, P. et al. Avian schistosomes and outbreaks of cercarial dermatitis. Clin. Microbiol. Rev. 28, 165–190 (2015).
PubMed  PubMed Central  Article  Google Scholar 
Brant, S. V. et al. An approach to revealing blood fluke life cycles, taxonomy, and diversity: Provision of key reference data including DNA sequence from single life cycle stages. J. Parasitol. 92, 77–88 (2006).
CAS  PubMed  Article  Google Scholar 
Brant, S. V. & Loker, E. S. Discovery-based studies of schistosome diversity stimulate new hypotheses about parasite biology. Trends Parasitol. 29, 449–459 (2013).
PubMed  PubMed Central  Article  Google Scholar 
Lorenti, E., Brant, S. V, Gilardoni, C., Diaz, J. I. & Cremonte, F. Two new genera and species of avian schistosomes from Argentina with proposed recommendations and discussion of the polyphyletic genus Gigantobilharzia (Trematoda, Schistosomatidae). Parasitology. 149, 1–59 (2022).
Article  Google Scholar 
Khalil, L. F. Family Schistosomatidae Stiles & Hassall, 1898. Keys Trematoda 1, 419–432 (2002).
Article  Google Scholar 
Snyder, S. D. & Loker, E. S. Evolutionary relationships among the Schistosomatidae (Platyhelminthes: Digenea) and an Asian origin for Schistosoma. J. Parasitol. 86, 283–288 (2000).
CAS  PubMed  Article  Google Scholar 
Brant, S. V. et al. Cercarial dermatitis transmitted by exotic marine snail. Emerg. Infect. Dis. 16, 1357 (2010).
PubMed  PubMed Central  Article  Google Scholar 
Leigh, W. H. The morphology of Gigantobilharzia huttoni (Leigh, 1953) an avian schistosome with marine dermatitis-producing larvae. J. Parasitol. 41, 262–269 (1955).
CAS  PubMed  Article  Google Scholar 
Ewers, W. H. A new intermediate host of schistosome trematodes from New South Wales. Nature 190, 283–284 (1961).
ADS  CAS  PubMed  Article  Google Scholar 
Rudolphi, K. A. Entozoorum synopsis cui accedunt mantissa duplex et indices locupletissimi. (Sumtibus A. Rücker, 1819).
Odhner, T. Zum natürlichen System der digenen Trematoden. V. Zool. Anz. 41, 54–71 (1912).
Google Scholar 
Farley, J. A review of the family Schistosomatidae: Excluding the genus Schistosoma from mammals. J. Helminthol. 45, 289–320 (1971).
CAS  PubMed  Article  Google Scholar 
Penner, L. R. The biology of a marine dermatitis-producing schistosome cercaria from Batillaria minima (Gmelin). J. Parasitol. 39, 19–20 (1953).
Google Scholar 
Al-Kandari, W. Y., Al-Bustan, S. A., Isaac, A. M., George, B. A. & Chandy, B. S. Molecular identification of Austrobilharzia species parasitizing Cerithidea cingulata (Gastropoda: Potamididae) from Kuwait Bay. J. Helminthol. 86, 470 (2012).
CAS  PubMed  Article  Google Scholar 
Martin, W. E. An annotated key to the cercariae that develop in the snail Cerithidea californica. Bull South Calif. Acad. Sci. 71, 39–43 (1972).
Google Scholar 
Holliman, R. B. Larval trematodes from the Apalachee Bay area, Florida, with a checklist of known marine cercariae arranged in a key to their superfamilies. Tulane Stud. Zool. 9, 1–74 (1961).
Google Scholar 
Short, R. B. & Holliman, R. B. Austrobilharzia penneri, a new schistosome from marine snails. J. Parasitol. 47, 447–450 (1961).
Article  Google Scholar 
Lindberg, W. F. P. D. R. Phylogeny and Evolution of the Mollusca (Univ of California Press, 2008).
Google Scholar 
Chong-ti, T. Philophthalmid larval trematodes from Hong Kong and the coast of south China. In The Marine Flora and Fauna of Hong Kong and Southern China II: Proceedings of the Second International Marine Biological Workshop Hong Kong, 2–24 April 1986 Vol. 1, 213 (Hong Kong University Press, 1990).
Taraschewski, H. Investigations on the prevalence of Heterophyes species in twelve populations of the first intermediate host in Egypt and Sudan. J. Trop. Med. Hyg. 88, 265–271 (1985).
CAS  PubMed  Google Scholar 
Reid, D. G. & Ozawa, T. The genus Pirenella Gray, 1847 (= Cerithideopsilla Thiele, 1929) (Gastropoda: Potamididae) in the Indo-West Pacific region and Mediterranean Sea. Zootaxa 4076, 1–91 (2016).
PubMed  Article  Google Scholar 
Vahidi, F., Fatemi, S. M. R., Danehkar, A., Mashinchian, A. & Nadushan, R. M. Benthic macrofaunal dispersion within different mangrove habitats in Hara Biosphere Reserve, Persian Gulf. Int. J. Environ. Sci. Technol. 17, 1295–1306 (2020).
CAS  Article  Google Scholar 
Nazeer, Z. et al. Macrofaunal assemblage in the intertidal area of Saudi Arabian Gulf Coast. Reg. Stud. Mar. Sci. 47, 101954 (2021).
Google Scholar 
Snyder, S. D. Phylogeny and paraphyly among tetrapod blood flukes (Digenea: Schistosomatidae and Spirorchiidae). Int. J. Parasitol. 34, 1385–1392 (2004).
CAS  PubMed  Article  Google Scholar 
Al-Zaidan, A. S. Y., Kennedy, H., Jones, D. A. & Al-Mohanna, S. Y. Role of microbial mats in Sulaibikhat Bay (Kuwait) mudflat food webs: Evidence from δ13C analysis. Mar. Ecol. Prog. Ser. 308, 27–36 (2006).
ADS  CAS  Article  Google Scholar 
Bearup, A. J. A schistosomc larva from the marine snail Pyrazus australisas a cause of cercarial dermatitis in man. Med. J. Aust. 1, 955–960 (1955).
Article  Google Scholar 
Grodhaus, G. & Keh, B. The marine, dermatitis-producing cercaria of Austrobilharzia variglandis in California (Trematoda: Schistosomatidae). J. Parasitol. 44, 633–638 (1958).
CAS  PubMed  Article  Google Scholar 
Sindermann, C. J. Ecological studies of marine dermatitis-producing schistosome larvae in northern New England. Ecology 41, 678–684 (1960).
Article  Google Scholar 
Pinto, H. A., Pulido-Murillo, E. A., de Melo, A. L. & Brant, S. V. Putative new genera and species of avian schistosomes potentially involved in human cercarial dermatitis in the Americas, Europe and Africa. Acta Trop. 176, 415–420 (2017).
PubMed  Article  Google Scholar 
Hechinger, R. F. & Lafferty, K. D. Host diversity begets parasite diversity: Bird final hosts and trematodes in snail intermediate hosts. Proc. R. Soc. B Biol. Sci. 272, 1059–1066 (2005).
Article  Google Scholar 
Aldhoun, J. A. & Horne, E. C. Schistosomes in South African penguins. Parasitol. Res. 114, 237–246 (2015).
PubMed  Article  Google Scholar 
Vanstreels, R. E. T. et al. Schistosomes and microfilarial parasites in Magellanic penguins. J. Parasitol. 104, 322–328 (2018).
CAS  PubMed  Article  Google Scholar 
Brant, S. V. & Loker, E. S. Can specialized pathogens colonize distantly related hosts? Schistosome evolution as a case study. PLoS Pathog. 1, e38 (2005).
PubMed Central  Article  CAS  Google Scholar 
Blair, D., Davis, G. M. & Wu, B. Evolutionary relationships between trematodes and snails emphasizing schistosomes and paragonimids. Parasitology 123, 229–243 (2001).
Article  Google Scholar 
Miller, H. M. Jr. & Northup, F. E. The seasonal infestation of Nassa obsoleta (Say) with larval trematodes. Biol. Bull. 50, 490–508 (1926).
Article  Google Scholar 
Chu, G. & Cutress, C. E. Human dermatitis caused by marine organisms in Hawaii. In Proceedings of the Hawaiian Academy of Science. 29th Annual Meeting (1953–54) (1954).
Szidat, L. Investigaciones sobre Cercaria chascomusi n. sp. Agente causal de una nueva enfermedad humana en la Argentina: La dermatitis de los bañistas de la laguna Chascomús. Bol Mus Argent Cienc Nat Bernardino Rivadavia 18, 1–16 (1958).
Google Scholar 
ITO, J. Studies on the morphology and life cycle of Pseudobilharziella corvi Yamaguti, 1941 (Trematoda: Schistosomatidae). Jpn. J. Med. Sci. Biol. 13, 53–58 (1960).
Article  Google Scholar 
Karamian, M. et al. Parasitological and molecular study of the furcocercariae from Melanoides tuberculata as a probable agent of cercarial dermatitis. Parasitol. Res. 108, 955–962 (2011).
PubMed  Article  Google Scholar 
Leedom, W. S. & Short, R. B. Cercaria pomaceae sp. n., a dermatitis-producing schistosome cercaria from Pomacea paludosa, the Florida apple snail. J. Parasitol. 67, 257–261 (1981).
Article  Google Scholar 
Aldhoun, J. A., Faltýnková, A., Karvonen, A. & Horák, P. Schistosomes in the North: A unique finding from a prosobranch snail using molecular tools. Parasitol. Int. 58, 314–317 (2009).
CAS  PubMed  Article  Google Scholar 
Horák, P., Kolářová, L. & Adema, C. M. Biology of the schistosome genus Trichobilharzia. (2002).
Martorelli, S. R. Sobre una cercaria de la familia Schistosomatidae (Digenea) parásita de Chilina gibbosa Sowerby, 1841 en el lago Pellegrini, Provincia de Río Negro, República Argentina. Neotrópica 30, 97–106 (1984).
Google Scholar 
Braun, M. Zur Revision der Trematoden der Vögel II. Zentralblatt fur Bakteriol. Abth I(29), 895–897 (1901).
Google Scholar 
Cheatum, E. L. Dendritobilharzia anatinarum n. sp., a blood fluke from the mallard. J. Parasitol. 27, 165–170 (1941).
Article  Google Scholar 
Leite, A. C. R., Costa, H. M. D. A. & Costa, J. O. Trichobilharzia jequitibaensis sp. n (Trematoda, Schistosomatidae) in Cairina moschata domestica (Anatidae). Rev. Bras. Biol. 38, 843–846 (1978).
Google Scholar 
McLeod, J. A. Two new schistosomid trematodes from water-birds. J. Parasitol. 23, 456–466 (1937).
Article  Google Scholar 
Ebbs, E. T. et al. Schistosomes with wings: How host phylogeny and ecology shape the global distribution of Trichobilharzia querquedulae (Schistosomatidae). Int. J. Parasitol. 46, 669–677 (2016).
PubMed  Article  Google Scholar 
Flores, V., Viozzi, G., Casalins, L., Loker, E. S. & Brant, S. V. A new schistosome (Digenea: Schistosomatidae) from the nasal tissue of South America black-necked swans, Cygnus melancoryphus (Anatidae) and the endemic pulmonate snail Chilina gibbosa. Zootaxa 4948, zootaxa-4948 (2021).
Article  Google Scholar 
Kolářová, L., Horák, P., Skírnisson, K., Marečková, H. & Doenhoff, M. Cercarial dermatitis, a neglected allergic disease. Clin. Rev. Allergy Immunol. 45, 63–74 (2013).
PubMed  Article  CAS  Google Scholar 
QGIS.org, QGIS 3.4. QGIS Geographic Information System. QGIS Association. http://www.qgis.org (2019).
Tkach, V., Grabda-Kazubska, B., Pawlowski, J. & Swiderski, Z. Molecular and morphological evidence for close phylogenetic affinities of the genera Macrodera, Leptophallus, Metaleptophallus and Paralepoderma [Digenea, Plagiorchiata]. Acta Parasitol. 44, 3 (1999).
Google Scholar 
Tkach, V. V., Littlewood, D. T. J., Olson, P. D., Kinsella, J. M. & Swiderski, Z. Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Syst. Parasitol. 56, 1–15 (2003).
PubMed  Article  Google Scholar 
Littlewood, D. T. J., Curini-Galletti, M. & Herniou, E. A. The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Mol. Phylogenet. Evol. 16, 449–466 (2000).
CAS  PubMed  Article  Google Scholar 
Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A. & Littlewood, D. T. J. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int. J. Parasitol. 33, 733–755 (2003).
CAS  PubMed  Article  Google Scholar 
Bowles, J. & McManus, D. P. Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method. Mol. Biochem. Parasitol. 57, 231–239 (1993).
CAS  PubMed  Article  Google Scholar 
Miura, O. et al. Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). Int. J. Parasitol. 35, 793–801 (2005).
CAS  PubMed  Article  Google Scholar 
Kuraku, S., Zmasek, C. M., Nishimura, O. & Katoh, K. aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res. 41, W22–W28 (2013).
PubMed  PubMed Central  Article  Google Scholar 
Katoh, K., Rozewicki, J. & Yamada, K. D. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 20, 1160–1166 (2019).
CAS  PubMed  Article  Google Scholar 
Telford, M. J., Herniou, E. A., Russell, R. B. & Littlewood, D. T. J. Changes in mitochondrial genetic codes as phylogenetic characters: Two examples from the flatworms. Proc. Natl. Acad. Sci. 97, 11359–11364 (2000).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. jModelTest 2: More models, new heuristics and parallel computing. Nat. Methods 9, 772 (2012).
CAS  PubMed  PubMed Central  Article  Google Scholar 
Ronquist, F. et al. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).
PubMed  PubMed Central  Article  Google Scholar 
Miller, M. A., Pfeiffer, W. & Schwartz, T. The CIPRES science gateway: a community resource for phylogenetic analyses. In Proceedings of the 2011 TeraGrid Conference: Extreme Digital Discovery 1–8 (2011).
Rambaut, A. & Drummond, A. J. Tracer v1. 5 http://beast.bio.ed.ac.uk/Tracer (2009).
Huelsenbeck, J. P., Ronquist, F., Nielsen, R. & Bollback, J. P. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294, 2310–2314 (2001).
ADS  CAS  PubMed  Article  Google Scholar 
Rambaut, A. & Drummond, A. J. FigTree v1. 4. 2012. (2012).
Lockyer, A. E. et al. The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126, 203 (2003).
CAS  PubMed  Article  Google Scholar 
Walker, J. C. Austrobilharzia terrigalensis: A schistosome dominant in interspecific interactions in the molluscan host. Int. J. Parasitol. 9, 137–140 (1979).
Article  Google Scholar 
Appleton, C. C. Studies on austrobilharzia terrigalensis (trematoda: schistosomatidae) in the swan estuary, Western Australia: Observations on the biology of the cercaria. Int. J. Parasitol. 13, 239–247 (1983).
CAS  PubMed  Article  Google Scholar 
Appleton, C. C. Studies on Austrobilharzia terrigalensis (Trematoda: Schistosomatidae) in the Swan Estuary, Western Australia: Frequency of infection in the intermediate host population. Int. J. Parasitol. 13, 51–60 (1983).
CAS  PubMed  Article  Google Scholar 
Johnston, S. H. On the Trematodes of Australian Birds. (1916).
Appleton, C. C. Observations on the histology of Austrobilharzia terrigalensis (Trematoda: Schistosomatidae) infection in the silver gull, Larus novaehollandiae. Int. J. Parasitol. 14, 23–28 (1984).
Article  Google Scholar 
Bearup, A. J. Life cycle of Austrobilharzia terrigalensis Johnston, 1917. Parasitology 46, 470–479 (1956).
CAS  PubMed  Article  Google Scholar 
CAMismoN, G. M., Bacha Jr, W. J. & Stempen, H. The circumoval precipitate and cercarienhiillen reaktion of Austrobilharzia variglandis. In Proc. Helminthol. Soc. Wash Vol. 48, 202–208 (1981).
Zibulewsky, J., Fried, B. & Bacha Jr, W. J. Skin surface lipids of the domestic chicken, and neutral lipid standards as stimuli for the penetration response of Austrobilharzia variglandis cercariae. J. Parasitol. 68, 905–908 (1982).
CAS  PubMed  Article  Google Scholar 
Bacha, W. J., Roush, R. & Icardi, S. Infection of the gerbil by the avian schistosome Austrobilharzia variglandis (Miller and Northup 1926; Penner 1953). J. Parasitol. 68, 505–507 (1982).
CAS  Article  Google Scholar 
Wood, L. M. & Bacha Jr, W. J. Distribution of eggs and the host response in chickens infected with Austrobilharzia variglandis (Trematoda). J. Parasitol. 69, 682–688 (1983).
CAS  PubMed  Article  Google Scholar 
Sindermann, C. J. The ecology of marine dermatitis-producing schistosomes. I. Seasonal variation in infection of mud snails (Nassa obsoleta) with larvae of Austrobilharzia variglandis. J. Parasitol. 42, 27 (1956).
Google Scholar 
Cutress, C. E. Austrobilharzia variglandis (Miller and Northup, 1926) Penner, 1953,(Trematoda: Schistosomatidae) in Hawaii with notes on its biology. J. Parasitol. 40, 515–524 (1954).
PubMed  Article  Google Scholar 
Rohde, K. The bird schistosome Austrobilharzia terrigalensis from the Great Barrier Reef, Australia. Zeitschrift für Parasitenkd. 52, 39–51 (1977).
CAS  Article  Google Scholar 
Price, E. W. A synopsis of the trematode family Schistosomidae, with descriptions of new genera and species. Proc. United States Natl. Museum (1929).
McLeod, J. A. Studies on cercarial dermatitis and the trematode family Schistosomatidae in Manitoba. Can. J. Res. 18, 1–28 (1940).
Article  Google Scholar 
Keppner, E. J. Some internal parasites of the California gull Larus californicus Lawrence, in Wyoming. Trans. Am. Microsc. Soc. 92, 288–291 (1973).
CAS  PubMed  Article  Google Scholar 
Johnston, S. J. On the trematodes of Australian birds. J. R. Soc. New South Wales 50, 187–261 (1917).
Google Scholar 
Appleton, C. C. Studies on Austrobilharzia terrigalensis (Trematoda: Schistosomatidae) in the Swan Estuary, Western Australia: Infection in the definitive host, Larus novaehollandiae. Int. J. Parasitol. 13, 249–259 (1983).
CAS  PubMed  Article  Google Scholar 
Penner, L. R. The red-breasted merganser as a natural avian host of the causative agent of clam diggers’ itch. J. Parasitol. 39, 20 (1953).
Google Scholar 
Johnston, T. H. Bather’s itch (schistosome dermatitis) in the Murray Swamps, South Australia. Trans. R. Soc. South Aust. 65, 276–284 (1941).
Google Scholar 
Witenberg, G. & Lengy, J. Redescription of Ornithobilharzia canaliculata (Rud.) Odhner, with notes on classification of the genus Ornithobilharzia and the subfamily Schistosomatinae (Trematoda). Isr. J. Zool. 16, 193–204 (1967).
CAS  PubMed  Google Scholar 
Curtis, L. A. Ilyanassa obsoleta (Gastropoda) as a host for trematodes in Delaware estuaries. J. Parasitol. 83, 793–803 (1997).
CAS  PubMed  Article  Google Scholar 
Curtis, L. A. & Tanner, N. L. Trematode accumulation by the estuarine gastropod Ilyanassa obsoleta. J. Parasitol. 85, 419–425 (1999).
CAS  PubMed  Article  Google Scholar 
Barber, K. E. & Caira, J. N. Investigation of the life cycle and adult morphology of the avian blood fluke Austrobilharzia variglandis (Trematoda: Schistosomatidae) from Connecticut. J. Parasitol. 81, 584–592 (1995).
CAS  PubMed  Article  Google Scholar 
Leighton, B. J. et al. Schistosome dermatitis at Crescent Beach, preliminary report. Environ. Heal. Rev. 48, 5–13 (2004).
Google Scholar 
Ferris, M. & Bacha Jr, W. J. Response of leukocytes in chickens infected with the avian schistosome Austrobilharzia variglandis (Trematoda). Avian Dis. 30, 683–686 (1986).
CAS  PubMed  Article  Google Scholar 
Stunkard, H. W. & Hinchliffe, M. C. The life-cycle of Microbilharzia variglandis (== Cercaría varíglandis Miller and Northup, 1926), an avian schistosome whose larvae produce’swimmer’s itch’of ocean beaches. Anat. Rec. 3, 529–530 (1951).
Google Scholar 
Stunkard, H. W. & Hinchliffe, M. C. The morphology and life-history of Microbilharzia variglandis (Miller and Northup, 1926) Stunkard and Hinchliffe, 1951, avian blood-flukes whose larvae cause” swimmer’s itch” of ocean beaches. J. Parasitol. 38, 248–265 (1952).
CAS  PubMed  Article  Google Scholar 
Penner, L. R. Experimental infections of avian hosts with Cercaria littorinalinae Penner, 1950. J. Parasitol. 39, 20 (1953).
Google Scholar 
Faust, E. C. Notes on Ornithobilharzia odhneri n. sp. from the Asiatic Curlew. J. Parasitol. 11, 50–54 (1924).
Article  Google Scholar 
Sousa, W. P. Interspecific antagonism and species coexistence in a diverse guild of larval trematode parasites. Ecol. Monogr. 63, 103–128 (1993).
Article  Google Scholar 
Chu, G. W. T. C. First report of the presence of a dermatitis-producing marine larval schistosome in Hawaii. Science 115, 151–153 (1952).
ADS  CAS  PubMed  Article  Google Scholar 
Canestri-Trotti, G., Fioravanti, M. L. & Pampiglione, S. Cercarial dermatitis in Italy. Helminthologia 38, 245 (2001).
Google Scholar 
Penner, L. R. Cercaria littorinalinae sp. nov., a dermatitis-producing schistosome larva from the marine snail, Littorina planaxis Philippi. J. Parasitol. 36, 466–472 (1950).
CAS  PubMed  Article  Google Scholar 
Abdul-Salam, J. & Sreelatha, B. S. Description and surface topography of the cercaria of Austrobilharzia sp. (Digenea: Schistosomatidae). Parasitol. Int. 53, 11–21 (2004).
CAS  PubMed  Article  Google Scholar 
Kinsella, J. M. & Forrester, D. J. Parasitic helminths of the common loon, Gavia immer, on its wintering grounds in Florida. Helminthol. Soc. Washingt. 66, 1–6 (1999).
Google Scholar 
Appleton, C. C. The eggs of some blood-flukes (Trematoda: Schistosomatidae) from South African birds. Afr. Zool. 17, 147–150 (1982).
Google Scholar 
Appleton, C. C. Occurrence of avian Schistosomatidae (Trematoda) in South African birds as determined by a faecal survey. Afr. Zool. 21, 60–67 (1986).
Google Scholar 
Courtney, C. H. & Forrester, D. J. Helminth parasites of the brown pelican in Florida and Louisiana. (1973).
Morales, G. A., Helmboldt, C. F. & Penner, L. R. Pathology of experimentally induced schistosome dermatitis in chickens: the role of Ornithobilharzia canaliculata (Rudolphi, 1819) Odhner 1912 (Trematoda: Schistosomatidae). Avian Dis. 262–276 (1971).
Travassos, L., Freitas, J. F. & Kohn, A. Trematódeos do Brazil. Mem. Inst. Oswaldo Cruz 67, 1–886 (1969).
CAS  PubMed  Google Scholar 
Saidov, Y. S. Gel’mintofauna ryb i ryboyadnykh ptits Dagestana (Helminthofauna of Fish and Ichthyophagous Birds of Dagestan). Candidate Thesis, VIGIS (1953).
Bykhovskaya-Pavlovskaya, I. E. et al. Key to parasites of freshwater fishes of the USSR, Academy of Science of the USSR. Zool. Inc (1962).
Leonov, V. A. New trematodes of ichthyophagus birds. Uchenye Zapiski Gorkovskogo Gosudarstvennogo Peda-gogicheskogo Instituta 19, 43–52 (1957).
Google Scholar 
Macro, J. K. Revision of Ornithobilharzia canaliculata (Rudolphi, 1819) (Trematoda: Schistosomatidae). Helminthologia 4, 303–311 (1963).
Google Scholar 
Bykhovskaya-Pavlovskaya, I. E. Trematode fauna of birds of Leningrad region. In Contrib. to Helminthol. Publ. to Commem. 75th Birthd. KI Skryabin.] Izd. Akad. Nauk SSSR, Moscov 85–92 (1953).
Santoro, M. et al. Helminth community structure of the Mediterranean gull (Ichthyaetus melanocephalus) in Southern Italy. J. Parasitol. 97, 364–366 (2011).
CAS  PubMed  Article  Google Scholar 
Sanmartín, M. L., Cordeiro, J. A., Alvarez, M. F. & Leiro, J. Helminth fauna of the yellow-legged gull Larus cachinnans in Galicia, north-west Spain. J. Helminthol. 79, 361–371 (2005).
PubMed  Article  Google Scholar 
Panova, L. G. On the trematode fauna of sea-gulls of the Don district. Trudy Leningrad. Gosudarstv. Vet. Inst. 1(1), 52–62 (1927) (in Russian).
Google Scholar 
Travassos, L. Contribucoes ao conhecimento dos Schistosomatidae. Sobre (Rudolphi, 1819). Rev. Bras. Biol. 2, 473–476 (1942).
Google Scholar 
Rind, S. The blood fluke Ornithobilharzia canaliculata (Rudolphi, 1819) (Trematoda: Schistosomatidae) from the gull Larus dominicanus at Lyttelton, New Zealand. (1984).
Szidat, L. Vergleichende helminthologische Untersuchungen an den argentinischen Grossmowen Larus marinus dominicanus Lichtenstein und Larus ridibundus maculipennis Lichtenstein neuen Beobachtungen uber die Artbildung bei Parasiten. Zeitschrift für Parasitenkd. 24, 351–414 (1964).
CAS  Google Scholar 
Parona, C. & Ariola, V. Bilharzìa kowalewskii n. sp. nel Larus melanocephalus [Nota preventiva]. Atti. Soc. Ligust. Sc. Nat. e Georg 7, 114–116 (1896).
Google Scholar 
Jothikumar, N. et al. Real-time PCR and sequencing assays for rapid detection and identification of avian schistosomes in environmental samples. Appl. Environ. Microbiol. 81, 4207–4215 (2015).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 
Shigin A.A. The helminth fauna of the Rybinsk Reservoir. Author’s abstract of dissertation, (1954).
Witenberg, G. Studies on the trematode—family Heterophyidae. Ann. Trop. Med. Parasitol. 23, 131–239 (1929).
Article  Google Scholar 
Bush, A. O. & Forrester, D. J. Helminths of the white ibis in Florida. Proc. Helminthol. Soc. Wash. 43, 17–23 (1976).
Google Scholar 
Mamaev, Y. L. Helminth fauna of Galliformes and Charadriiformes in Eastern Siberia. Tr. Gelmintol. Lab. Akad. Nauk SSSR (1959).
Download references
We are indebted to professor Martin Wahl, GEOMAR Helmholtz Centre for Ocean Research, Kiel, for his generous support during the study. We sincerely thank Mr. Amir Reza Heidari Motahar for the immense help during the field work in Iran. We gratefully acknowledge the help provided by Mrs. Mehregan Heidari and all members of the Parasitology group at Hormozgan University in Iran for the support with logistics. MK benefited from “Studienstiftung des deutschen Volkes” PhD fellowship and research grant by benthic ecology group of GEOMAR. SG was supported by the National Research Foundation of Korea Grant #2021H1D3A2A02081767.
Department of Marine Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, Düsternbrooker Weg 20, 24105, Kiel, Germany
Maral Khosravi
Department of Coastal Systems, NIOZ Royal Netherlands Institute for Sea Research, P.O. Box 59, 1790, AB, Den Burg Texel, The Netherlands
David W. Thieltges
Infectious and Tropical Diseases Research CenterHormozgan Health Institute, Hormozgan University of Medical Sciences, Bandar Abbas, Iran
Jebreil Shamseddin
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113, Sofia, Bulgaria
Simona Georgieva
Department of Parasitology, School of Medicine, Chungbuk National University, Chungdae-ro 1, Seowon-gu, 28644, Cheongju, South Korea
Simona Georgieva
You can also search for this author in PubMed Google Scholar
You can also search for this author in PubMed Google Scholar
You can also search for this author in PubMed Google Scholar
You can also search for this author in PubMed Google Scholar
M.K. and S.G.: conceived the study, obtained samples, carried out the sequencing, performed analyses prepared the first draft of the manuscript. M.K., D.T., J.S., S.G. discussed the results and helped draft the manuscript. All authors read and approved the final manuscript.
Correspondence to Maral Khosravi.
The authors declare no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
Reprints and Permissions
Khosravi, M., Thieltges, D.W., Shamseddin, J. et al. Schistosomes in the Persian Gulf: novel molecular data, host associations, and life-cycle elucidations. Sci Rep 12, 13461 (2022). https://doi.org/10.1038/s41598-022-17771-2
Download citation
Received: 04 March 2022
Accepted: 30 July 2022
Published: 05 August 2022
DOI: https://doi.org/10.1038/s41598-022-17771-2
Anyone you share the following link with will be able to read this content:
Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.
Advertisement
Advanced search
Scientific Reports (Sci Rep) ISSN 2045-2322 (online)
© 2022 Springer Nature Limited
Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

source

About the Author

Leave a Reply

error: Konten dilindungi !!
adana eskort - eskişehir eskort - eskort mersin