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Trematoda: Digenea © Institute of Parasitology, Biology Centre CAS >;+'-F;+-& doi: '+'99''G;+'-+-& http://folia.paru.cas.cz Research Article Morphological and molecular data for three species of the Microphallidae (Trematoda: Digenea) in Australia, [ Maritrema brevisacciferum Shimazu et Pearson, 1991 and Microphallus minutus Johnston, 1948 Olena Kudlai';&, Scott C. Cutmore4 and Thomas H. Cribb4 1!5$ D5#67= ; JK#M$= 3 Q7R6UQ= 4 The University of Queensland, School of Biological Sciences, Brisbane, Queensland, Australia Abstract: Cercariae and metacercariae of three species of the Microphallidae Y#'Z;+were found in snails and crustaceans 776#[!Maritrema brevisacciferum Shimazu et Pearson, 1991 and Microphallus minutus ]'Z9<, which have previously been reported in Queensland, were found as cercariae in the tateid gastropod Posticobia brazieri (Smith) and as metacercariae of M. brevisacciferum in the atyid shrimp Caridina indistincta Calman and of M. minutus[Cherax dispar 6$. Combined analysis of morphological and molecular data, based on newly Y!;;<!JR$7Y[[@ termediate hosts of M. brevisacciferum and M. minutus.[_ gen. sp., were found in P. brazieri and C. indistincta. The sequences of metacercarial isolates from both hosts were identical. The data _#`#7`? Keywords: #JRj`76# Y _ Y# 'Z;+ However, despite the numerous records of microphal@ globally distributed family of digeneans that parasitise [#` #7 xJ7$ ;++<{ larval stages from intermediate hosts from this region. but have their greatest richness in birds and mammals. _ '; # 7 @ The life cycles of microphallids involve gastropods, most@ =77$@ 7$ ` [ ish water snail, Coxiella badgerensis Johnston (see John@ and crustaceans as second intermediate hosts. Previous 'Z9<J7$'ZF<'ZFZ!'Z*9 studies from Australia have reported 35 microphallid spe@ 'Z<& J7$ 'ZZ+ ! 'ZZ' ';xAtriophallophorusJ7$6 J7$'ZZF{Y@ 'ZF9=Basantisia'Z&<=Endocotyle Belopol'skaya, `7x'Z*<{`@ 'Z-;= Gynaecotyla ~ 'Z&Z= Levinseniella Stiles [ 'Z+'= Maritrema R 'Z+*= Microphallus cerithiid gastropod, Clypeomorus batillariaeformis Habe 'Z+'= Mochliscotrema J7$ 'Z<F= et Kosuge (as Cerithium moniliferum Kiener) from the Pseudolevinseniella Y 'Z--= Queenslandisia Pearson 6Y# J7$'Z<*=Rhyncostophallus Deblock et Canaris, literature of microphallid cercariae from freshwater snails 'ZZ*=ThulakiotremaJ7$B#'ZZ+{ 6 `# Maritrema mainly from birds, with few species known from mammals poulini`@#;+'9 x$'Z--J7$'ZF<'ZFZ_`@ metacercariae of MicrophallusΣ#Τ`7 'Z<F!'ZZ'{ from a freshwater snail, Potamopyrgus antipodarum !#$&'&*++-5$ D5#6789;+&<***-9&*=>?89;+@&<@-&'+&<<=B@$D This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. '+'99''G;+'-+-& >`icrophallid larvae in Australia Table 1. Host data, geographical origin and GenBank accession numbers for digenean species used in phylogenetic analyses. Species Host Country GenBank 6 N;<! Maritrema Nicoll, 1907 M. arenaria Hadley et Castle, 1940 Semibalanus balanoides Belfast Lough, Northen Ireland ~;;+F;Z Y$x;++&{ (Linnaeus) M. brevisacciferum Shimazu et Pearson, Posticobia brazieri (Smith) Brisbane, Australia Y&--<'Z Present study 1991 M. brevisacciferum Caridina indistincta Calman Brisbane, Australia Y&--<'< Present study M. eroliae Yamaguti, 1939 Clypeomorus bifasciatus Shuwaikh Bay, Kuwait ]><;F;9* @x;+''{ (Sowerby) M. heardi (Kinsella et Deblock, 1994) Oryzomys palustris (Harlan) >M! ~;;+F&; Y$x;++&{ M. neomiY$'ZZ< Neomys anomalus Cabrera K$$6M$ >'-'Z;* Y$x;+++{ M. novaezealandense Martorelli, Zeacumantus subcarinatus Portobello Bay, Dunedin, New ]'99'*< Presswellx;+'9{ >7_et;++9 (Sowerby) Zealand M. oocysta (Lebour, 1907) Hydrobia ulvae (Pennant) Belfast Lough, Northen Ireland ~;;+F&+ Olsonx;+03) M. poulini`@ Paracorophium excavatum Lake Waihola, Waihola, New KJ144177 Presswellx;+'9{ et#;+'9 (Thomson) Zealand M. prosthometra Deblock et Heard, 1970 Oryzomys palustris >M! ~;;+F&' Y$x;++&{ M. subdolum Jägerskiöld, 1909 Hydrobia ulvae Kandalaksha Bay, White Sea, _-<9'&- $#x;+';{ 6 M. deblocki`@ Anas platyrhynchos Linnaeus B New KJ144173 Presswellx;+'9{ et #;+'9 Zealand Microphallus Ward, 1901 M. abortivus Deblock, 1974 Hydrobia ulvae Belfast Lough, Northen Ireland ~;;+F;F Y$x;++&) M. basodactylophallusx'ZFZ{ Oryzomys palustris >M! ~;;+F;< Y$x;++&{ M. fusiformis6'ZF& Hydrobia ulvae Belfast Lough, Northen Ireland ~;;+F&& Y$x;++&{ M. minutus ]'Z9< Posticobia brazieri Brisbane, Australia Y&--<;& Present study M. minutus Cherax dispar6$ Brisbane, Australia Y&--<;; Present study M. primasx]$'Z+<{ Hydrobia ulvae Belfast Lough, Northen Ireland ~;;+F;* Y$x;++&{ M. similis (Jägerskiöld, 1900) Carcinus maenas (Linnaeus) Belfast Lough, Northen Ireland ~;;+F;- Y$x;++&{ M. triangulatus $#'Z<9 Somateria mollissima Bona@ Yamskaya Bay, Sea of Okhotsk, _-<9'&Z $#x;+';{ parte et Gray 6 Microphallus sp. Somateria mollissima Cape Taygonos, Sea of _-<9'9; $#x;+';{ $$6 Microphallus sp. Austrolittorina cincta (Quoy et R6$, New Zealand ]<F<;'* O’Dwyerx;+'9{ Gaimard) Microphallidae gen. sp. Posticobia brazieri Brisbane, Australia Y&--<;+ Present study Microphallidae gen. sp. Caridina indistincta Brisbane, Australia Y&--<;' Present study Outgroup Paralecithodendrium chilostomum Viviparus viviparus (Linnaeus) Kyiv, Ukraine ]';F*;- x;+'-{ x_'<&'{ MATERIALS AND METHODS x {R`Kx;+';` ;+'9{ Sample collection During a study of parasites infecting freshwater inverte@ ! ` >7@ 776#7 ;+'- 7 7 6# of the tateid gastropod Posticobia brazieri (Smith) and the _ $ x;*&+'F!= '-;---+B{ 7$ crustaceans Caridina indistincta Calman and Cherax dis- x;*9F'F!= '-;9'+;B{ > $ x;*;<-<!= par 6$`7`# '-;9++9B{ 99<+ Posticobia brazieri ` ?@ stages of species belonging to the family Microphallidae. &< Caridina indistincta, 34 Macrobrachium Detailed morphological study and comparative analyses tolmerum6$Cherax dispar`?_@ 7 `@7 j 7@ gill Creek and Churchbank Weir. Y!;;<!JR# [Maritrema brevisac- Morphological data ciferum Shimazu et Pearson, 1991, Microphallus minutus In the laboratory, snails were placed individually in plastic con@ ]'Z9<__@ ``? ae of M. brevisacciferum and M. minutus have previous@ of naturally emerged cercariae. Infected gastropods were subse@ ly been recorded in prawns Caridina niloticax6?{ quently dissected to determine the nature of the intramolluscan [C. dispar#76# stages. Cercariae`?#follow@ x!'ZZ'{7[ ing staining with neutral red, under slight coverslip pressure. Pho@ of neither species has been reported. This paper provides tomicrographs of live isolates (cercariae and metacercariae) were morphological descriptions and genetic characterisation of $ ` R$ J ! J!@Q xR$ the larval stages of the three microphallid species discov@ Y$]{ @; @ 76#7 croscope. Measurements were taken from pictures of live material >;+'-F;+-& ;'& '+'99''G;+'-+-& >`icrophallid larvae in Australia with SPOT™ imaging software. All measurements are in micro@ was then trimmed to the length of the shortest sequence. Phy@ metres and are given as a range followed by the mean and the logenetic analysis was carried out using Bayesian inference (BI) number of measurements taken (n) in parentheses. Drawings are _?Q$x_Q{Y7@ based on digital images of live cercariae and metacercariae. tution model, the general time reversible model, with estimates of #7@# Molecular data x Y688 {`5_Y;`xJ@ Total genomic DNA was isolated using phenol/chloroform 7;+';{`_@ ?jx!7$6;++'{Y `x#&;&{x6j;+';{6B! J'MJ&;<!7JR` x_ ;+'+{ ` ` 7 [ Q!M- x-@Y Y Y@ F#j'++ ~YY @&=Q`;+++{'-++6x-@ @ ncat = 4, shape = estimate, inferrates = yes and basefreq = em@ YYY YY @&=!Y$;++'{ pirical. Markov chain Monte Carlo (MCMC) chains were run for Y!;`[&!x-@ Y@ '+++++++ @$ ` Y Y Y Y Y @&= ` 'ZZ&{ [*-` Y!;;x-@Y YY YYYYYYYY @&=77 7Σ7@Τ;-++Y7 'ZZ<{67;<!Y!;` `[7#@ `#;+)-)-&_Yj6@ ation dropped well below 0.01 at the end of the run. ML analysis x{+*-3x'+{+;-3 `_Q#&+x ;+'+{ Yjx_Yj(JR{;3 Y 7R? JRx?'+{;+3`@ !jGG```@GR #(M6B(`[`@ _?Q$`7@ _]6Y@'-+ ing 100 bootstrap pseudoreplicates. Trees were visualised using Y ` [ ` ;<! >Y#'9`x67;+';{ Z-9`7&+ Z-'-F'*; RESULTS ?;`7Z-@ B?99<+#Posticobia brazie- '--9-[*;? ri 76#7 9Y`[`Y!; Queensland revealed infections with digeneans from eight Z- & families. Nine infections consistent with species of the 9-;*;?Z+`7 _`[7 9Z-9--+9- emerged cercariae. Metacercariae of Maritrema brevisac- *;?Z+`7&+Z-@ ciferum and Microphallidae gen. sp. were found in Carid- ;+-;;+*;?Z+ ina indistincta= metacercariae of Microphallidae gen. sp. `7[*;?- were also found in huge numbers in the tissues of a single [ JR ` [ !QYB P. brazieri. Metacercariae of Microphallus minutus were 6 R@ recovered from Cherax dispar. No specimen of Macrobra- j[JR` chium tolmerum was infected by digenean metacercariae. Dye™ v.3.1 chemistry following the manufacturer’s recommen@ Descriptions of the mature cercariae and metacercariae of 6[ these digeneans are provided below. `;<!JR&++>x-@ Y@ Y YY@&= Q` ;+++{ BJ; > Microphallidae Y#'Z;+ x-@YY Y Y YYY @&= Q` ;+++{Y!; 'x-@ Y @ Genus Maritrema Nicoll, 1907 YYY @&=$'ZZ<{j@ ` 6> Maritrema brevisacciferum Shimazu et Pearson, 1991 &*&+? j !j( # >' 4.5 (GeneCodes Corp.) was used to assemble and edit contiguous j $ 7 ? j Description of cercaria x7 ;+ # this study are shown in Table 1. emerged specimens from P. brazieri from Moggill Creek): R`;<!JR#Mari- ! ? # @ trema brevisacciferum,
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