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Taxonomic Revision of Species of Haematoloechus Looss, 1899

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Taxonomic Revision of Species of Haematoloechus Looss, 1899 Zootaxa 4526 (3): 251–302 ISSN 1175-5326 (print edition) http://www.mapress.com/j/zt/ Article ZOOTAXA Copyright © 2018 Magnolia Press ISSN 1175-5334 (online edition) https://doi.org/10.11646/zootaxa.4526.3.1 http://zoobank.org/urn:lsid:zoobank.org:pub:4DF63CE5-4838-46CA-BB0E-2F91841D5CB1 Taxonomic revision of species of Haematoloechus Looss, 1899 (Digenea: Plagiorchioidea), with molecular phylogenetic analysis and the description of three new species from Mexico VIRGINIA LEÓN-RÈGAGNON1, 2 & JANET TOPAN2 1Estación de Biología Chamela, Instituto de Biología, Universidad Nacional Autónoma de México, A.P. 21, San Patricio, Jalisco, México, CP 48980. E-mail: [email protected] 2Centre for Biodiversity Genomics, University of Guelph, 50 Stone Road East, Guelph, ON, N1G 2W1, Canada Abstract Lung flukes of the genus Haematoloechus Looss, 1899 are common parasites of anurans worldwide, but the taxonomy of the group has been confusing. In this taxonomic revision, 89 species of Haematoloechus (= Pneumonoeces Looss, 1902, Ostioloides Odening, 1960, Ostiolum Pratt, 1903, Skrjabinoeces Sudarikov, 1950, Neohaematoloechus Odening, 1960, Metahaematoloechus Yamaguti, 1971) are listed. Of these, 70 are considered valid, three are species inquirendae (H. legrandi Mañé–Garzón & Gil, 1959, H. latoricensis Kozák, 1968 & H. vitelloconfluentum (Rai, 1962) Saeed, Al–Barwari & Al-Harmni, 2007), one is a nomen nudum H. sudarikovi Belouss, 1962, 14 are junior synonyms and one belongs to Osti- oloides. This publication also describes three new species, H. occidentalis n. sp., H. veracruzanus n. sp. and H. mexicanus n. sp., parasitizing species of Rana Linnaeus in Mexico and redescribes Haematoloechus caballeroi (Skrjabin & Antipin, 1962) Yamaguti, 1971. The phylogenetic hypotheses based on sequences of mitochondrial and ribosomal DNA of Hae- matoloechus spp. show that genera proposed on the basis of morphological characters are not supported. The host records for species of Haematoloechus, together with the phylogenetic hypothesis of the genus, suggest that this host-parasite as- sociation predates the ranid diversification in the Cretaceous. Key words: 28S rDNA, Amphibia, Biogeography, Coevolution, COI, Haematoloechidae, Haematoloechus mexicanus n. sp., Haematoloechus occidentalis n. sp., Haematoloechus veracruzanus n. sp., host list, Mexico, Platyhelminthes, Rani- dae, Phylogram, species list Introduction Members of the genus Haematoloechus Looss, 1899 are parasites in the lungs of anurans, known from every continent except Antarctica. First reported in the early 19th Century, the type species was originally named Distomum variegatum Rudolphi, 1819 but was transferred to the newly erected genus Haematoloechus by Looss (1899), who also described two European species, H. similis Looss, 1899, and H. asper Looss, 1899. In 1902, the genus was renamed as Pneumonoeces Looss, 1902 because a hemipteran genus had previously been named Haematoloecha Stal. Although Harwood (1932) and Ingles (1932) independently reinstated Haematoloechus, some other authors continued to use Pneumonoeces (Skrjabin & Antipin 1962). Some current members of this genus were placed in other genera mostly based on the varying arrangement of the uterine loops. Ostiolum Pratt, 1903 was, for example, proposed for species lacking extracecal longitudinal uterine loops (Pratt 1903), Pneumobites Ward, 1917 for those with longitudinal uterine loops extending to the pre-acetabular region of body, with H. longiplexus as its type species (Ward 1917). Skrjabinoeces Sudarikov, 1950 was proposed for species with the vitelline follicles placed anteriorly to testes with H. similis as its type species (Sudarikov 1950). Odening (1958) recognized the genus Ostiolum and three subgenera within Haematoloechus: Haematoloechus, Anomolecithus Odening, 1958 and Skrjabinoeces Odening, 1958 based on the arrangement of the vitelline follicles, and later erected Neohaematoloechus Odening, 1960 for those species lacking ventral sucker, with H. neivai (Travassos & Artigas, 1927) Ingles, 1933 as its type species (Odening 1960). This author also erected the genus Accepted by N. Dronen: 17 Oct. 2018; published: 30 Nov. 2018 251 Ostioloides Odening, 1960 to include Haematoloechus rappiae (Szidat, 1932) Yamaguti, 1958. Skrjabin & Antipin (1962) continued to use the name Pneumonoeces, and recognized Ostiolum, Skrjabinoeces and Neohaematoloechus as distinct genera. From the previous taxonomic proposals, Yamaguti (1971) only recognized Neohaematoloechus, Ostioloides and erected a new genus, Metahaematoloechus Yamaguti, 1971, for species with extracecal testes, with H. exoterorchis Rees, 1964 as the type species. He placed all other species within Haematoloechus, recognizing two subgenera: Haematoloechus and Skrjabinoeces. Based on extensive studies of the host use and geographic distribution of North American species of Haematoloechus, Kennedy (1980a; 1980b) concluded that most characters used to differentiate species were examples of intraspecific variation. As a result, he synonymized 9 of the 15 species known at that time from the U.S.A. and Canada (Kennedy 1981). Unfortunately, the limited detail in the original descriptions (Stafford 1902; Seely 1906), and the lack of type material for some species, has led to confusion in the identification and delineation of taxa. More recent research, using molecular characters to complement morphology, has revalidated species once relegated to synonymy. These studies aided the identification of morphological characters valuable in differentiating species, and revealed that some genera erected to include species of Haematoloechus are polyphyletic (León-Règagnon et al. 1999, 2001; Snyder & Tkach 2001; León-Règagnon & Paredes-Calderón 2002; León-Règagnon & Brooks 2003; Bolek & Janovy 2007a; León- Règagnon 2010; Zamparo et al. 2011). Molecular evidence has also shown that H. complexus (Seely, 1906) a species prevalent in the eastern U.S.A. (Bolek & Janovy 2007a) and previously thought to occur in Mexico (Caballero 1942b; León-Règagnon 1992; Pérez-Ponce de León et al. 2000) is actually a complex of sibling species whose conserved morphology makes their differentiation difficult (León-Règagnon et al. 1999; León-Règagnon 2003, 2010). The present study revises the taxonomy of the genus in the light of recent molecular and morphological studies, describes three new species of Haematoloechus that parasitize frogs in Mexico, and provides a list of the species historically assigned to Haematoloechus and related genera. Materials and methods Original descriptions and taxonomic literature related to the genus were reviewed while voucher and type material were examined from the following collections: Colección Nacional de Helmintos (CNHE), Instituto de Biología, Universidad Nacional Autónoma de México; Canadian Museum of Nature Parasite Collection (CMNPA); U. S. National Parasite Collection at the National Museum of Natural History (NMNH); Natural History Museum, UK (NHM); and the Colecão Helmintológica do Instituto Oswaldo Cruz, Brazil (IOC). Host nomenclature and higher classification of anurans was based on the Amphibian Species of the World 6.0 (http://research.amnh.org/vz/ herpetology/amphibia/) (Frost 2018). Classification and nomenclature of the Ranidae Batsch was based on Hillis & Wilcox (2005) and Bossuyt et al. (2006). Considering the length of this manuscript, the genera Haematoloechus and Rana are not spelled out for each species the first time it is presented, but rather the abbreviations H. and R. are used to avoid excessive repetition. From 1997 to 2017, specimens of Lake Lerma salamander Ambystoma lermaense (Taylor), Rio Grande leopard frog Rana berlandieri Baird, Brown´s leopard frog R. brownorum Sanders, American bullfrog R. catesbeiana Shaw, green frog R. clamitans Latreille, Patzcuaro leopard frog R. dunni Zweifel, Forrer´s leopard frog R. cf. forreri, big–footed leopard frog R. megapoda Taylor, Montezuma leopard frog R. montezumae Baird, Transverse Volcanic leopard frog R. neovolcanica Hillis & Frost, Amazon River frog R. palmipes Spix, showy leopard frog R. spectabilis Hillis & Frost, common marsh frog R. vaillanti Brocchi, and Zweifel´s frog R. zweifeli Hillis, Frost & Webb were collected from varied localities in Mexico and Canada under scientific collection permits FAUT0056 (Mexico) and AUP3762 (Canada) issued to VLR and Paul D. N. Hebert. Amphibians were captured manually or using dip nets and killed by an overdose of sodium pentobarbital or double pithing. Helminthological examination was completed within 24 hours of capture. Digeneans recovered from these frogs were initially placed in saline (0.65%) solution, examined for preliminary identification and separated by morphotypes. For detailed morphometric study they were fixed by sudden immersion in hot 4% formaldehyde, and then preserved in 70% ethanol. Specimens were stained with Mayer's paracarmine or Gomori´s trichrome, dehydrated, cleared in methyl salicylate, and mounted in Canada balsam. Some specimens were permanently mounted between cover slips and held in Cobb slides. Measurements are presented as the range with means in parentheses and expressed in micrometers, unless otherwise stated. Figures were drawn with the aid of a drawing tube. 252 · Zootaxa 4526 (3) © 2018 Magnolia Press LEÓN-RÈGAGNON & TOPAN Total DNA was extracted from whole digeneans using standard glass fibre methods (Ivanova et al. 2006) or standard phenol extraction (Hillis et al. 1996). After purification, 2 µL of DNA was added to a PCR reaction
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