Neotropical Turtle Blood Flukes: Two New Genera and Species from the Amazon River Basin with a Key to Genera and Comments on a Marine-Derived Parasite Lineage in South America

Bullard, Stephen A.; Roberts, Jackson R.; Warren, Micah B.; Dutton, Haley R.; Whelan, Nathan V.; Ruiz, Carlos F.; Platt, Thomas R.; Tkach, Vasyl V.; Brant, Sara V.; Halanych, Kenneth M.

doi:10.1645/19-27

Cited by 16 publications

(8 citation statements)

References 88 publications

(133 reference statements)

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“…The two gray arrows denote the two major derived nodes leading to two simultaneous and independent radiations, one predominantly in birds the other predominantly in mammals. Spirorchiidae samples fall into two clades concordant with the results of Bullard et al [ 61 ], with a South American species recovered from a freshwater turtle, as sister to Schistosomatidae.…”

Section: Resultssupporting

confidence: 86%

Phylogenomics and Diversification of the Schistosomatidae Based on Targeted Sequence Capture of Ultra-Conserved Elements

Ebbs

Loker

et al. 2022

Pathogens

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Schistosomatidae Stiles and Hassall 1898 is a medically significant family of digenetic trematodes (Trematoda: Digenea), members of which infect mammals or birds as definitive hosts and aquatic or amphibious gastropods as intermediate hosts. Currently, there are 17 named genera, for many of which evolutionary interrelationships remain unresolved. The lack of a resolved phylogeny has encumbered our understanding of schistosomatid evolution, specifically patterns of host-use and the role of host-switching in diversification. Here, we used targeted sequence capture of ultra-conserved elements (UCEs) from representatives of 13 of the 17 named genera and 11 undescribed lineages that are presumed to represent either novel genera or species to generate a phylogenomic dataset for the estimation of schistosomatid interrelationships. This study represents the largest phylogenetic effort within the Schistosomatidae in both the number of loci and breadth of taxon sampling. We present a near-comprehensive family-level phylogeny providing resolution to several clades of long-standing uncertainty within Schistosomatidae, including resolution for the placement of the North American mammalian schistosomes, implying a second separate capture of mammalian hosts. Additionally, we present evidence for the placement of Macrobilharzia at the base of the Schistosoma + Bivitellobilharzia radiation. Patterns of definitive and intermediate host use and a strong role for intermediate host-switching are discussed relative to schistosomatid diversification.

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Section: Resultssupporting

confidence: 86%

Phylogenomics and Diversification of the Schistosomatidae Based on Targeted Sequence Capture of Ultra-Conserved Elements

Ebbs

Loker

et al. 2022

Pathogens

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“…P. expansa, P. unifilis; adult; stomach, Loreto (MUSM-HEL 2975) (Tantaleán et al, 2011) (Bullard et al, 2019).…”

Section: Resultsunclassified

“…Paratamatam iquitosiensis Bullard & Roberts, 2019 C. fimbriata; adult; blood vessels of kidney and mesentery; Loreto (03°45 ′ S, 73°14 ′ W) (holotype, USNM 1557313; paratype, USNM 1557314-1557319) (Bullard et al, 2019).…”

Section: Resultsmentioning

confidence: 99%

A checklist of helminths associated with reptiles (Tetrapoda: Reptilia) from Peru

et al. 2022

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An annotated checklist of the helminth parasites associated with reptiles from Peru is provided, as the result of a compilation of parasitological papers published between 1963 and January 2022 and records of species deposited in national and international collections. The list provides data on hosts, developmental stage, sites of infection, geographical distribution in Peruvian territory, code of material deposited in helminthological collections, references and taxonomic notes. The database includes records of 106 different species of helminth parasites (82 nominal species and 24 taxa identified at the generic level), the majority in the adult stage. These helminth parasites come from 18 of the 25 official Peruvian regions. Nematodes have the highest richness in number of species (79 species), followed by trematodes (17 species) and cestodes (nine species). The acanthocephalans are represented by only one species. The parasites with the highest number of records were Physaloptera retusa Rudolphi, 1819 (11 hosts), Physalopteroides venancioi (Lent, Freitas & Proença, 1946) (nine hosts), Strongyluris oscari Travassos, 1923 (seven hosts), and Parapharyngodon scleratus Travassos, 1923 (five hosts), all of which are nematodes. The 106 taxa of helminth parasites have been reported infecting 55 species of reptiles in Peru, distributed in 34 genera and 14 families. The reptile species harbouring the highest number of helminth parasites are the yellow-footed tortoise Chelonoidis denticulatus (Linnaeus) with 18 species (three trematodes and 15 nematodes), followed by the Peru desert tegu Dicrodon guttulatum Duméril & Bibron (Teiidae) with 11 species (three cestodes and eight nematodes) and the yellow-spotted Amazon River turtle Podocnemis unifilis Troschel (Podocnemididae) with 10 species (five trematodes and five nematodes). Of the 524 species of reptiles reported in Peru, only 55 (>10%) are reported as hosts of helminths representing a small proportion considering the great variety of reptile hosts that inhabit the various tropical and subtropical geographical areas of Peru.

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“…Relatively little is known about liolopid infections especially in turtles, with only 3 publications total that have detailed an infection in a turtle ( Odhner, 1912 ; Travassos, 1922 ; Skrjabin, 1962 ); only L. dollfusi and the new species reportedly mature in turtles exclusively ( Table 1 ). This is astonishingly low sampling effort given the extremely high diversity of extant freshwater turtle species ( Rhodin et al, 2017 ; Bullard et al, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

“…Measurements were obtained with a calibrated ocular micrometer (as straight-lines along the course of each duct) and are reported in micrometres (μm) as the range followed by the mean, +/− standard deviation, and sample size in parentheses. Two specimens were processed for scanning electron microscopy (SEM) as per Bullard et al (2019) . Type and voucher materials of the new species were deposited in the National Museum of Natural History's Invertebrate Zoology Collection (USNM, Smithsonian Institution, Washington, D. C.).…”

Section: Methodsmentioning

confidence: 99%

Paraharmotrema karinganiense n. gen., n. sp. (Digenea: Liolopidae) infecting the intestine of serrated hinged terrapin (Pelusios sinuatus), east African black mud turtle (Pelusios subniger), and South African helmeted turtle (Pelomedusa galeata) and a phylogenetic hypothesis for liolopid genera

Dutton

Preez

Urabe

et al. 2022

International Journal for Parasitology: Parasites and Wildlife

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We herein describe Paraharmotrema karinganiense n. gen., n. sp. Dutton & Bullard (Liolopidae Dollfus, 1934) from specimens infecting the intestine of the serrated hinged terrapin ( Pelusios sinuatus ), east African black mud turtle ( Pelusios subniger ) (both Nwanedzi River, Mozambique), and South African helmeted terrapin ( Pelomedusa galeata ) (North-western Zululand, KwaZulu-Natal Province, South Africa). The new genus can be easily differentiated from the other accepted liolopid genera ( Liolope Cohn, 1902; Helicotrema Odhner, 1912; Harmotrema Nicoll, 1914; Dracovermis Brooks & Overstreet, 1978) by the combination of having a linguliform body approximately 6–9 × longer than wide, tegumental spines/scales, a minute ventral sucker located in the anterior 1/7−1/8 of the body, deeply lobed testes that are transverse and abut the caeca (spanning the intercaecal space), a uterus that is lateral to the anterior testis (not ventral to the anterior testis), a lobed ovary that is dextral and nearest the posterior testis, and a vitellarium that does not extend anteriad to the level of the ventral sucker and that does not fill the intercaecal space. Nucleotide sequences of large subunit ribosomal DNA ( 28S ) and internal transcribed space region ( ITS2 ) from all analyzed specimens of the new species were identical, respectively; the 28S sequences differed from that of Liolope copulans Cohn, 1902 and from that of Harmotrema laticaudae Yamaguti, 1933 by 103 (8%) and 105 (8%) nucleotides, respectively. The 28S phylogenetic analysis recovered the new genus sister to a clade comprising L. copulans and H. laticaudae . A key to liolopid genera is provided herein. The present study comprises the first nucleotide-based phylogenetic placement of Harmotrema and first record of a liolopid from South Africa or Mozambique. It is the first proposal of a new liolopid genus in 43 yrs, and it documents a second liolopid genus from P. subniger while tripling the number of liolopid turtle hosts reported from the continent of Africa.

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Neotropical Turtle Blood Flukes: Two New Genera and Species from the Amazon River Basin with a Key to Genera and Comments on a Marine-Derived Parasite Lineage in South America

Cited by 16 publications

References 88 publications

Phylogenomics and Diversification of the Schistosomatidae Based on Targeted Sequence Capture of Ultra-Conserved Elements

Phylogenomics and Diversification of the Schistosomatidae Based on Targeted Sequence Capture of Ultra-Conserved Elements

A checklist of helminths associated with reptiles (Tetrapoda: Reptilia) from Peru

Paraharmotrema karinganiense n. gen., n. sp. (Digenea: Liolopidae) infecting the intestine of serrated hinged terrapin (Pelusios sinuatus), east African black mud turtle (Pelusios subniger), and South African helmeted turtle (Pelomedusa galeata) and a phylogenetic hypothesis for liolopid genera

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