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Discovery of a new genus and species of Allocreadiidae (Trematoda) in Mexico: Mesoamericatrema magnisacculus n. gen. n. sp

B. Mendoza-Garfias
B. Mendoza-Garfias
, 
J. G. García-Teh
J. G. García-Teh
, 
J. M. Caspeta-Mandujano
J. M. Caspeta-Mandujano
, 
V. M. Vidal-Martínez
V. M. Vidal-Martínez
 and 
D. I. Hernández-Mena
D. I. Hernández-Mena
   | Dec 17, 2022
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Article Category: Research Article
Published Online: Dec 17, 2022
Page range: 284 - 300
Received: Aug 03, 2022
Accepted: Aug 30, 2022
DOI: https://doi.org/10.2478/helm-2022-0029
Keywords
© 2022 B. Mendoza-Garfias, J. G. García-Teh, J. M. Caspeta-Mandujano, V. M. Vidal-Martínez, D. I. Hernández-Mena, published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Fig. 1

Mesoamericatrema magnisacculus n. sp.: a) Dorso-ventral view of the holotype (scale bar= 200 μm); a) Lateral view of a paratype (scale bar= 200 μm); c) and d) Ventral view of two different male genitalia, showing the cirrus sac containing the seminal vesicle, the pars prostatica, and the ejaculatory duct (scale bar= 100 μm). The seminal vesicle is embedded in a very thick sac.
Mesoamericatrema magnisacculus n. sp.: a) Dorso-ventral view of the holotype (scale bar= 200 μm); a) Lateral view of a paratype (scale bar= 200 μm); c) and d) Ventral view of two different male genitalia, showing the cirrus sac containing the seminal vesicle, the pars prostatica, and the ejaculatory duct (scale bar= 100 μm). The seminal vesicle is embedded in a very thick sac.

Fig. 2

Scanning electron micrographs of Mesoamericatrema magnisacculus n. sp.: A) ventral view of the entire body (scale bar= 100 μm); B) and C) ventral view of two different oral suckers showing the oral papillae (6 external anterior in blue arrows, 4 internal in green arrows and 5 external posterior in red arrows; scale bar= 25 μm); d) ventral view of the ventral sucker (scale bar= 25 μm); e) ventral view of terminal excretory pore at posterior end of hindbody (scale bar= 25 μm); f) close-up of an external oral papilla (scale bar= 5 μm); g) sperm leaving the genital pore (scale bar= 5 μm); h) egg released through the genital pore (scale bar= 25 μm).
Scanning electron micrographs of Mesoamericatrema magnisacculus n. sp.: A) ventral view of the entire body (scale bar= 100 μm); B) and C) ventral view of two different oral suckers showing the oral papillae (6 external anterior in blue arrows, 4 internal in green arrows and 5 external posterior in red arrows; scale bar= 25 μm); d) ventral view of the ventral sucker (scale bar= 25 μm); e) ventral view of terminal excretory pore at posterior end of hindbody (scale bar= 25 μm); f) close-up of an external oral papilla (scale bar= 5 μm); g) sperm leaving the genital pore (scale bar= 5 μm); h) egg released through the genital pore (scale bar= 25 μm).

Fig. 3

Photographs where the size of the cirrus bag is observed with respect to the size of the body. The length of the ejaculatory duct, the pars prostatica and the seminal vesicle, which is surrounded by a thick wall of the sac, are also observed; a), b) and c) paratypes stained with Mayer’s paracarmine; d) paratype stained with Gomori’s trichrome. Scale bar= 50 μm.
Photographs where the size of the cirrus bag is observed with respect to the size of the body. The length of the ejaculatory duct, the pars prostatica and the seminal vesicle, which is surrounded by a thick wall of the sac, are also observed; a), b) and c) paratypes stained with Mayer’s paracarmine; d) paratype stained with Gomori’s trichrome. Scale bar= 50 μm.

Fig. 4

Maximum Likelihood phylogenetic tree of the 28S gene for Allocreadiidae species, showing the position of the new genus that is highlighted in bold red font (–ln= 9888.861897). Numbers near internal nodes indicate bootstrap support and posterior probabilities values.
Maximum Likelihood phylogenetic tree of the 28S gene for Allocreadiidae species, showing the position of the new genus that is highlighted in bold red font (–ln= 9888.861897). Numbers near internal nodes indicate bootstrap support and posterior probabilities values.

Fig. 5

Phylogenetic tree of the species of Allocreadiidae with Neotropical distribution, indicating their definitive hosts and the families of fish to which they belong with Neotropical affinity.
Phylogenetic tree of the species of Allocreadiidae with Neotropical distribution, indicating their definitive hosts and the families of fish to which they belong with Neotropical affinity.

Trematode species included in phylogenetic analyses with the 28S rRNA gene. The accession number of the Genbank sequences, the host and the locality where the sequenced specimens were collected are shown.

Species Author GenBank Host Locality Sequence Reference
ALLOCREADIIDAE Looss, 1902
Acrolichanus auriculatum (Wedl, 1858) Skvortsov, 1927 MN524579 Acipenser schrenckii Russia Atopkin et al., 2020
Allocreadium gotoi (Hasegawa & Ozaki, 1926) Shimazu, 1988 LC215274 Misgurnus anguillicaudatus Japan: Nagano, liyama, Midori Shimazu, 2017
Allocreadium isoporum (Looss, 1894) Looss, 1902 GU462125 Alburnus alburnus Russia: Lake Oster, Karelia Petkeviciüte et al., 2010
Allocreadium lobatum Wallin, 1909 EF032693 Semotilus corporalis USA Curran et al., 2006
Allocreadium neotenicum Peters, 1957 JX977132 Hydroporus rufifrons United Kingdom: Lake District, Cumbria Bray et al., 2012
Bunodera acerinae Roitman & Sokolov, 1999 GU462122 Gymnocephalus cernua Russia: River Tvertsa, upper Volga River basin Petkeviciüte et al., 2010
Bunodera eucaliae (Miller, 1936) Miller, 1940 DQ029329 Culaea inconstans Canada: Brokenhead River, Manitoba Choudhury and Leon-Regagnon, 2005
Bunodera inconstans (Lasee, Font & Sutherland, 1988) Brooks, 1992 DQ029330 Culaea inconstans Canada: Brokenhead River, Manitoba Choudhury and Leon-Regagnon, 2005
Bunodera luciopercae (Müller, 1776) Lühe, 1909 GU462113 Sphaerium rivicola Russia: River Tvertsa, upper Volga River basin Petkeviciüte et al., 2010
Bunodera mediovitellata Tsimbalyuk & Roitman, 1966 DQ029332 Gasterosteus aculeatus Canada: Little Campbell River, B. C. Choudhury and Leon-Regagnon, 2005
Bunodera sacculata Van Cleave & Mueller, 1932 DQ029333 Perea fluviatilis Canada: Lake Sasajewun, Algonquin Park, Ontario Choudhury and Leon-Regagnon, 2005
Bunodera vytautasi Atopkin, Sokolov, Shedko, Vainutis & Orlovskaya, 2018 MG262545 Pungitius pungitius Canada: Magadan region, Chernoe Lake Atopkin et al., 2018
Crepidostomum affine Tkach, Curran, Bell & Overstreet, 2013 KF250358 Hiodon tergisus USA: Pearl River,Mississippi Tkach, et a/., 2013
Crepidostomum auritum (MacCallum, 1919) KF250357 Aplodinotus grunniens USA: Pearl River,Mississippi Tkach, et a/., 2013
Crepidostomum cooperi Hopkins, 1932 DQ029328 Percopsis omiscomaycus Canada: Lake Winnipeg, Manitoba Choudhury and Leon-Regagnon, 2005
Crepidostomum cornutum (Osborn, 1903) Stafford, 1904 EF032695 Lepomis gulosus USA Curran et al., 2006
Crepidostomum farionis (Müller, 1780) Lühe, 1909 FR821399 Oncorhynchus masou Russia Atopkin and Shedko, 2014
Crepidostomum illinoiense Faust, 1918 KF356372 Hiodon alosoides USA: Red Lake River,Minnesota Tkach, et a/., 2013
Crepidostomum metoecus (Braun, 1900) Braun, 1900 FR82140 Salvelinus leucomaensis Russia Atopkin and Shedko, 2014
Crepidostomum nemachilus Krotov, 1959 FR821408 Salvelinus leucomaensis Russia Atopkin and Shedko, 2014
Crepidostomum oschmarini Zhokhov & Pugacheva, 1998 MH159994 Pisidium casertanum Lithuania: River Nedzinge Petkeviciüte et al., 2018
Creptotrema astyanace (Scholz, Aguirre-Macedo & Choudhury, 2004) Franceschini, Aguiar, Zago, de Oliveira Fadel Yamada, Bertholdi Ebert & da Silva, 2021 HQ833707 Astyanax aeneus Costa Rica: Guanacaste Curran etal., 2011
Creptotrema stenopteri (Mane-Garzon & Gascon, 1973) Franceschini, Aguiar, Zago, de Oliveira Fadel Yamada, Bertholdi Ebert & da Silva, 2021 MN822005 Charax stenopteri Argentina: Buenos Aires, Punta Lara Montes et al., 2021
Creptotrema conconae Franceschini, Aguiar, Zago, de Oliveira Fadel Yamada, Bertholdi Ebert & da Silva, 2021 OK044374 Imparfinis mirini Brazil: Upper Parana River basin Franceschini et al., 2021
Creptotrema creptotrema Travassos, Artigas & Pereira, 1928 OK044371 Megaleporinus elongatus Brazil: Mogi-Guacu River, Upper Parana River basin Franceschini et al., 2021
Creptotrema funduli Mueller, 1934 JQ425256 Fundulus notatus USA: Mississippi, Biloxi River, Harrison County Curran et al., 2012
Creptotrema guacurarii (Montes, Barneche, Croci, Balcazar, Almiron, Martorelli & Perez-Ponce de Leon, 2021) Franceschini, Aguiar, Zago, de Oliveira Fadel Yamada, Bertholdi Ebert & da Silva, 2021 MN822004 Characidium heirmostigmata Argentina: Misiones, Parque Nacional Iguazu Montes et al., 2021
Creptotrema lobata (Hernändez-Mena, Lynggaard, Mendoza-Garfias & Perez- Ponce de Leon, 2016) Franceschini, Aguiar, Zago, de Oliveira Fadel Yamada, Bertholdi Ebert & da Silva, 2021 KX954170 Brycon guatemalensis Mexico: Tenosique, Chiapas Hernändez-Mena etal., 2016
Creptotrema megacetabularis Franceschini, Aguiar, Zago, de Oliveira Fadel Yamada, Bertholdi Ebert & da Silva, 2021 OK044375 Auchenipterus osteomystax Brazil: Upper Parana River basin Franceschini et al., 2021
Creptotrema schubarti Franceschini, Aguiar, Zago, de Oliveira Fadel Yamada, Bertholdi Ebert & da Silva, 2021 OK044373 Characidium schubarti Brazil: Upper Parana River basin Franceschini et al., 2021
Creptotrema tica (Hernandez Mena, Pinacho-Pinacho, Garcia-Varela, Mendoza- Garfias & Perez-Ponce de Leon, 2018) Franceschini, Aguiar, Zago, de Oliveira Fadel Yamada, Bertholdi Ebert & da Silva, 2021 MH997001 Gymnotus maculosus Costa Rica: Creek at Pitaya, Guanacaste Hernändez-Mena etal., 2019
Creptotrema totonacapanensis (Razo-Mendivil, Mendoza-Garfias, Perez- Ponce de Leon & Rubio-Godoy, 2014) Franceschini, Aguiar, Zago, de Oliveira Fadel Yamada, Bertholdi Ebert & da Silva, 2021 KF631417 Astyanax mexicanus Mexico: Filipinas, Veracruz Razo-Mendivil et al., 2014b
Creptotrematina aguirrepequenoi Jimenez-Guzman, 1973 HQ833708 Astyanax aeneus Costa Rica: Guanacaste Curran etal., 2011
Creptotrematina batalhensis Dias & Abdallah in Alves Dias, Perez-Ponce de Leon, Almeida Camargo, Müller, Silva, Kozlowiski de Azevedo & Abdallah, 2020 MT512642 Astyanax lacustris Brazil: Batalha River Dias et al., 2020
Margotrema bravoae Lamothe-Argumedo, 1970 KT833278 Allotoca dugesii Mexico (Central region) Perez-Ponce de Leon et al., 2016
Margotrema resolanae Perez-Ponce de Leon, Martinez-Aquino & Mendoza-Garfias, 2013 KT833271 Xenotaenia resolanae Mexico (Central region) Perez-Ponce de Leon et al., 2016
Megalogonia ictaluri Surber, 1928 EF032694 Ictalurus punctatus USA: Pearl River, Mississippi Curran et al., 2006
Mesoamericatrema magnisacculus This study OP279638- OP279642 Atherinella alvarezi Mexico: Arroyo San Jose, Chiapas This study
Paracreptotrema blancoi Choudhury, Perez Ponce de Leon, Brooks & Daverdin, 2006 KT833285 Priapichthys annectens Costa Rica: Orosi River Perez-Ponce de Leon et al., 2016
Paracreptotrema rosenthali Bautista-Hernandez, Monks, Pulido-Flores & Miranda, 2015 KT833287 Xiphophorus malinche Mexico: Malila River, Hidalgo Perez-Ponce de Leon et al., 2016
Paracreptotrematoides heterandriae (Salgado-Maldonado, Caspeta-Mandujano & Vazquez, 2012) Perez Ponce de Leon, Pinacho-Pinacho, Mendoza-Garfias, Choudhury & Garcia-Varela, 2016 KF697693 Heterandria bimaculata Mexico: Agua Bendita, Xico, Veracruz Razo-Mendivil et al., 2014a
Pseudoparacreptotrema axtlaensis Mendoza-Garfias & Choudhury, 2020 MT180832 Agonostomus monticola Mexico: Axtla de Terrazas, San Luis Potosi Perez-Ponce de Leon et al., 2020
Pseudoparacreptotrema falciformis Hernändez-Mena & Pinacho-Pinacho, 2020 MT180829 Agonostomus monticola Mexico: Matias Romero, Oaxaca Perez-Ponce de Leon et al., 2020
Pseudoparacreptotrema macroacetabulata Perez Ponce de Leon, Pinacho-Pinacho, Mendoza-Garfias, Choudhury & Garcia-Varela, 2016 KT833322 Profundulus kreiseri Guatemala: Puente Sansare Perez-Ponce de Leon et al., 2016
Pseudoparacreptotrema pacificum Sereno-Uribe & Garcia-Varela, 2020 MT180810 Agonostomus monticola Costa Rica: Rio Lajas Perez-Ponce de Leon et al., 2020
Pseudoparacreptotrema profundulusi (Salgado-Maldonado, Caspeta-Mandujano & Martinez- Ramirez, 2011) Perez Ponce de Leon, Pinacho-Pinacho, Mendoza-Garfias, Choudhury & Garcia-Varela, 2016 KT833290 Profundulus sp. Mexico: Templo River, San Juan del Rio, Oaxaca Perez-Ponce de Leon et al., 2016
Wallinia anindoi Hernändez Mena, Pinacho-Pinacho, Garcia-Varela, Mendoza- Garfias & Perez-Ponce de Leon, 2018 MH997003 Astyanax aeneus Mexico: San Juan del Rio, Oaxaca Hernändez Mena et al., 2018
Wallinia brasiliensis Dias, Müller, Almeida, Silva, Azevedo, Perez-Ponce de Leon & Abdallah, 2018 MH520995 Astyanax fasciatus Brazil: Upper Paranä River Basin Dias et al., 2018
Wallinia caririensis Silva, Dias, Silva & Yamada, 2020 MW024866 Astyanax bimaculatus Brazil: Batateiras River da Silva et al., 2021
Wallinia chavarriae Choudhury, Daverdin & Brooks, 2002 HC833703 Astyanax aeneus Costa Rica: Animas River, Guanacaste Curran et al., 2011
Wallinia mexicana Perez-Ponce de Leon, Razo-Mendivil, Mendoza-Garfia, Rubio-Godoy & Choudhury, 2015 KJ535504 Astyanax mexicanus Mexico: Covadonga River, Durango Perez-Ponce de Leon et al., 2016
CALLODISTOMIDAE Odhner, 1910
Prosthenhystera caballeroi Jimenez-Guzmän, 1973 KM871185 Astyanax aeneus Costa Rica: Tampisquto River, Guanacaste Tkach and Curran, 2015
Prosthenhystera obesa (Diesing, 1850) Travassos, 1922 AY222206 Hoplias sp. Peru: Itaya River, Iquitos Olson et al., 2003
Prosthenhystera oonastica Tkach & Curran, 2015 KM871181 Pylodictis olivaris USA: Pearl River, Mississippi Tkach and Curran, 2015

Genetic distances between Mesoamericatrema magnisacculus n. gen. n. sp. and the Allocreadiidae species of the Neotropical clade in the 28S and ITS ribosomal genes (na= sequences not available in Genbank).

Species Mesoamericatrema magnisacculus
28S ITS
Creptotrema schubarti 5.63 na
Creptotrema guacurarii 5.37 na
Creptotrema creptotrema 5.53 na
Creptotrema tica 3.75 na
Creptotrema cf. stenopteri 5.01 na
Creptotrema megacetabularis 4.71 na
Creptotrema totonacapanensis 3.83 4.94
Creptotrema conconae 6.42 na
Creptotrema lobata 3.75 4.63
Creptotrema astyanace 3.79 4.40
Wallinia brasiliensis 5.20 na
Wallinia anindoi 5.43 na
Wallinia caririensis 6.24 na
Wallinia mexicana 5.76 na
Wallinia chavarriae 3.94 5.12
Creptotrematina batalhensis 5.46 4.81
Creptotrematina aguirrepequenoi 4.59 5.65
Paracreptotrema blancoi 3.91 7.29
Paracreptotrema rosenthali 5.69 8.27
Paracreptotrematoides heterandriae 4.62 4.34
Pseudoparacreptotrema axtlaense 5.03 na
Pseudoparacreptotrema falciforme 4.86 na
Pseudoparacreptotrema macroacetabulatum 3.93 7.56
Pseudoparacreptotrema pacificum 5.61 na
Pseudoparacreptotrema profundulusi 5.29 7.56
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