Skip to main content
NCBI home page
International Journal for Parasitology: Parasites and Wildlife logoLink to International Journal for Parasitology: Parasites and Wildlife
. 2024 Jul 2;24:100961. doi: 10.1016/j.ijppaw.2024.100961

Acanthoatractis xinguensis n. gen., n. sp. (Nematoda: Cosmocercoidea: Atractidae) parasite of yellow-spotted Amazon river turtle, Podocnemis unifilis Troschel (Testudines: Podocnemididae) in Brazilian Amazon

Ronald Ferreira Jesus 1,⁎, Bianca Nandyara 1, Jeannie Nascimento dos Santos 1, Francisco Tiago de Vasconcelos Melo 1
PMCID: PMC11280331  PMID: 39070049

Abstract

Nematodes collected from the stomach of the yellow-spotted turtle Podocnemis unifilis Troschel, 1848 (Testudinidae) in the Brazilian state of Pará are assigned to a new genus, allocated to the family Atractidae (Cosmocerdoidea). Acanthoatractis n. gen. differs from all other genera of Atractidae based on the combination of the following morphological characters: cephalic extremity surrounded by eight bifurcated, wrench-shaped sclerotized structures arranged in a circle; oral opening encircled by two sclerotized pieces with pointed ends and a median portion with a pair of hooks; in males the larger (left) spicule is narrower in the middle third and the gubernaculum is absent. The type species, Acanthoatractis xinguensis n. gen., n. sp., has nine pairs of caudal papillae and a single papilla anterior to the cloacal lip. The new species is the seventh record of an atractid genus parasitizing P. unifilis.

Keywords: Brazilian Amazon, Atractidae, Acanthoatractis xinguensis, Podocnemis unifilis, Turtle nematode

Graphical abstract

Image 1

Open in a new tab

Highlights

  • •

    A new genus and species of atractids parasitizing freshwater turtles from the Amazon region.

  • •

    Acanthoatractis n. gen. differs from all other genera by the shape of sclerotized structures on the cephalic end.

  • •

    This is the 27th genus of the family Atractidae.

  • •

    This is the seventh record of an atractid genus parasitizing Podocnemis unifilis.

1. Introduction

Nematodes of Atractidae Railliet, 1917 (Travassos, 1919) are frequently found parasitizing fish, amphibians, reptiles, and mammals. Currently, this family accommodate 27 valid genera, namely: Atractis Dujardin, 1845, Labiduris Schneider, 1866, Probstmayria Ransom, 1907, Crossocephalus Railliet, 1909, Cobboldina Leiper, 1911, Cyrtosomum Gedoelst, 1919, Rondonia Travassos, 1920, Leiperenia Khalil, 1922, Monhysterides Baylis and Daubney, 1922, Grassenema Petter, 1959, Paratractis Sarmiento, 1959, Nouvelnema Petter, 1959, Klossinemella Costa, 1961, Pseudatractis Yamaguti, 1961, Fitzsimmonsnema Petter, 1966, Orientatractis Petter, 1966, Pseudocyrtosomum Gupta and Johri, 1987, Buckleyatractis Khalil and Gibbons, 1988, Podocnematractis Gibbons, Khalil and Marinkelle, 1995, Diceronema Gibbons, Knapp and Krecek, 1996, Paraorientatractis Gibbons, Khalil and Marinkelle, 1997, Rhinoclemmysnema Gibbons and Platt, 2006, Pneumoatractis Bursey, Reavill and Greiner, 2009, Rhinoceronema Mondal and Manna, 2013, Hippopotamenema Mondal and Manna, 2015 and Vogtnema Jesus et al., 2022.

Podocnemis Wagler, 1830 comprises freshwater turtles endemic to northern South America (Ferrara et al., 2017). To date, six atractid genera have been reported from Podocnemis unifilis Troschel, 1848, including Buckleyatractis, Orientatractis, Paraorientatractis, Paratractis, Pneumoatractis, and Podocnematractis (Khalil and Gibbons, 1988; Gibbons et al., 1995, 1997; Bursey et al., 2009; Jesus et al., 2020). However, we found some atractid nematodes that we could not allocate to any already known genera of the family. Thus, we propose and describe a new genus and species based on light and scanning electron microscopy.

2. Materials and methods

Three specimens of Podocnemis unifilis were collected from the Xingu River (“Volta Grande” region), municipality of Vitória do Xingu, Pará, Brazil, during a survey of helminths in freshwater turtles. Hosts were anesthetized by injection of 2% ketamine and posteriorly euthanized by ketamine overdosage. The organs of the gastrointestinal tract (stomach, small and large intestines) were carefully removed, isolated in Petri dishes, and examined under a LEICA EZ4 stereomicroscope (Leica Microsystems, Wetzlar, Germany). Nematodes were washed in saline solution (NaCl 0.9%) and heat-killed in 70% ethanol. For morphological and morphometric analysis, the nematodes were cleared in 20% Aman's lactophenol, following a protocol adapted from Amato et al. (1991), and examined using an Olympus BX41 microscope (Olympus, Japan) with a drawing tube. Measurements are in micrometers unless otherwise indicated and are presented as the range followed by the mean in parentheses.

We selected six specimens (three males and three females) for scanning electron microscopy (SEM) analyses. The nematodes were post-fixed in 1% OsO4, dehydrated in a graded ethanol series (30–100%), critical point dried with CO2, and placed on aluminum stubs using carbon tape and sputter coated with gold/palladium. We analyzed the specimens under a Vega3 microscope (TESCAN, Brno, Czech Republic) with an acceleration voltage of 10 kV in the Laboratory of Cellular Structural Biology (LBE) at the Federal University of Pará (UFPa).

The type-material was deposited in the Invertebrate Collection of the Helminthological Collection of Oswaldo Cruz Institute (CHIOC), Brazil.

3. Results

3.1. Acanthoatractis Jesus and Melo n. gen

Diagnosis: Cosmocercoidea. Atractidae. Body medium-sized, tapering anteriorly, tail short and pointed with cuticle finely longitudinally striated. Lateral alae absent. Cephalic end surrounded by eight bifurcated sclerotized structures (two subdorsal pairs, two dorsolateral pairs, two subventral pairs, and two ventrolateral pairs) shaped like single-ended wrench, arranged in circle. These sclerotized structures equal, positioned on opposite sides in both transverse and longitudinal planes. Oral aperture small, terminal, and rectangular, surrounded by two sclerotized pieces (one ventral and one dorsal); each piece with pointed ends and median portion with pair of hooks; two large lateral amphids present. Esophagus divided into two parts; anterior esophagus (corpus) with distal bulb muscular, posterior esophagus (isthmus), ending in non-valvulated bulb; nerve ring encircling isthmus; excretory pore anterior to esophageal bulb. Male with nine pairs of caudal papillae; spicules unequal, only larger (left) one narrower in middle portion, lanceolate; gubernaculum absent. Female monodelphic, ovoviviparous with vulva close to anus.

Etymology: The name of the genus comes from the greek “acanth/o,” meaning spine or thorn, referring to the presence of spines on the cephalic end of the nematode.

3.2. Acanthoatractis xinguensis Jesus and Melo n. gen., n. sp.

3.2.1. General description

Medium-sized nematodes, body cylindrical, tapering to both extremities. Males and females similar in length without lateral alae. Esophagus divided into defined corpus, elongated isthmus, and a bulb. Nerve ring situated in middle of esophagus, at beginning of isthmus; deirids small, located just below nerve ring. Excretory pore anterior to esophageal bulb, opening surrounded by radial cuticle striations; pore opening into large chamber with transverse striations. Posterior end with short, pointed tail, ventrally curved in both sexes.

3.2.2. Male (based on holotype; 13 paratypes all adult males)

Total body length 4.21 (3.74–4.33) mm; width at esophago-intestinal junction 127 (97–127). Esophagus 548 (479–565) long with corpus, isthmus and bulb. Corpus 221 (198–221) long, distal bulb 58 (47–58) × 32 (29–36); isthmus including esophageal bulb 328 (266–357) long. Width of bulb 45 (38–52). Nerve ring, excretory pore and deirids at 240 (229–251), 411 (336–412) and 341 (326–367) respectively, from anterior end of body. Nine pairs of caudal papillae and one unpaired papillae anterior to cloacal lip: three subventral precloacal pairs, one subventral adcloacal pair, and five postcloacal pairs (first subventral, second subventral, third subventral, fourth subventral and fifth dorsolateral); phasmids ventrolateral, located between second and third pairs of postcloacal papillae 179 (177–209) (Fig. 1F; 3C). Spicules lanceolate, unequal, with transverse striations along its length, distal ends sharply pointed, larger (left) spicule narrower in middle third 343 (326–382) long, smaller (right) spicule 123 (110–149) long (Fig. 1E). Tail 317 (275–349) long (Fig. 1D–F; 3C).

Fig. 1.

Fig. 1

Open in a new tab

Line drawings of Acanthoatractis xinguensis n. gen., n. sp. (Male) (A) Cephalic extremity, apical view. (B) Cephalic extremity, apical view, highlighting the oral opening surrounded by sclerotized pieces and the distribution of open end wrench-shaped sclerotized structures. (C) Anterior extremity of body, ventral view. (D) Whole body, lateral view. (E) Details of spicules. (F) Posterior extremity of body, ventral view.

3.2.3. Female (based on allotype; 15 paratypes all adult females)

Total body length 4.01 (3.64–4.05) mm; body width at esophago-intestinal junction 126 (94–130). Esophagus 573 (485–573) long with corpus, isthmus and bulb. Corpus 217 (173–231) long, distal bulb 52 (44–56) × 30 (29–32); isthmus including esophageal bulb 356 (304–356) long. Width of bulb 54 (47–56). Nerve ring, excretory pore and deirids at 211 (211–259), 405 (344–405) and 371 (291–371) respectively, from anterior end of body. Phasmids located at 136 (132–140) from posterior end. Viviparous, vulva situated at 373 (301–373) from posterior end of body, from anus to vulva 47 (40–51). Muscular vagina anteriorly directed 41 (41–42). Monodelphic, prodelphic, uterus beginning in posterior flexion of vagina, directing anteriorly, containing one or two larvae (Fig. 2A and B; 3D). Tail 307 (256–332) long (Fig. 2B; 3D).

Fig. 2.

Fig. 2

Open in a new tab

Line drawings of Acanthoatractis xinguensis n. gen., n. sp. (Female) (A) Posterior extremity of body, region of vulva and anus, lateral view. (B) Reproductive tract showing monodelphic uterus, lateral view.

3.3. Taxonomic summary

Superfamily Cosmocercoidea Railliet, 1916.

Family Atractidae Railliet, 1917 (Travassos, 1919).

Acanthoatractis xinguensis Jesus and Melo n. gen., n. sp. (Fig. 1, Fig. 2, Fig. 3)

Fig. 3.

Fig. 3

Open in a new tab

Scanning electron micrographs of Acanthoatractis xinguensis n. gen., n. sp. (A) Male, cephalic extremity, subapical view. (B) Anterior extremity of body, ventrolateral view. Inset: Detail of deirid, lateral view (Scale-bar: 10 μm); Detail of excretory pore, ventral view (Scale-bar: 10 μm). (C) Posterior extremity of male, ventrolateral, distribution of caudal papillae (arrowheads). Detail of phasmid, ventrolateral view (Scale-bar: 5 μm); Postcloacal papillae, ventrolateral view (Scale-bar: 10 μm). (D) Posterior extremity of female, ventrolateral view, lines indicate vulva and anus. Abbreviations: Amphid, Am; anus, An; deirid, De; excretory pore, Ep; single median papilla, Sm; vulva, Vu.

Type-host: Podocnemis unifilis Troschel, 1848 (Chelonia: Testudinae).

Type-locality: Xingu River (“Volta Grande” region) (3°23′12.682″S 51°44′58.315″W), Municipality of Vitória do Xingu, Pará, Brazil.

Type-specimens: Holotype (CHIOC 39197a), allotype (CHIOC 39197b) and 28 paratypes (CHIOC 39197c-39197d) were deposited in the helminthological collection of Oswaldo Cruz Institute - Rio de Janeiro, Brazil.

Site of infection: Stomach.

Prevalence: 33% (1 infected/3 examined).

ZooBank registration: To comply with the regulations set out in article 8.5 of the amended 2012 version of the International Code of Zoological Nomenclature (ICZN, 2012), details of the new species have been submitted to ZooBank. The Life Science Identifier (LSID) for Acanthoatractis xinguensis n. gen., n. sp. Is urn: lsid: zoobank.org: act: ABE15A5D-A805-49BE-A544-DCBBDBA20EF6.

Etymology: The species was named after the Xingu River, the type locality.

4. Discussion

Jesus et al. (2022) proposed an identification key for Atractidae and listed 27 valid genera. Among these genera, Labeonema Puylaert, 1970 was included; however, molecular analyses indicated that the phylogenetic position of Labeonema is within Cosmocercidae Railliet, 1914 (see Saito et al., 2021). Therefore, in this study, we will consider 26 valid genera, listed in a table that includes type species, host, and biogeographic occurrence of Atractidae genera (see Table 1).

Table 1.

Genus, type-species, host and Biogeographic occurrence of Atractidae (26 valid genera are included here and the new genus) around the world.

Genus Type-species Hosts Biogeographic occurrence of species Reference
Acanthoatractis n. gen Acanthoatractis xinguensis n. gen., n. sp. Reptiles (Freshwater turtle) Neotropical This study
Atractis Atractis dactyluris Fish and reptiles (Freshwater turtle, tortoise and Squamata) Neotropical, Ethiopian, Oriental, Palaearctic Dujardin (1845)
Labiduris Labiduris gulosa Reptiles (Tortoise) Neotropical and Ethiopian Schneider (1866)
Probstmayria Probstmayria vivipara Mammals Neotropical Ransom (1907)
Crossocephalus Crossocephalus viviparus Mammals Oriental, Ethiopian Railliet (1909)
Cobboldina Cobboldina vivipara Mammals Oriental, Ethiopian Leiper (1911)
Cyrtosomum Cyrtosomum scelopori Reptiles (Squamata) Neotropical and Neartic Gedoelst (1919)
Rondonia Rondonia rondoni Peixes and anfíbios Neotropical and Australian Travassos (1920)
Leiperenia Leiperenia leiperi Mammals Ethiopian and oriental Khalil (1922)
Monhysterides Monhysterides piscicola Fish and reptiles (Freshwater turtle) Oriental and neotropical Baylis and Daubney (1922)
Grassenema Grassenema procaviae Mammals Ethiopian and oriental Petter (1959)
Paratractis Paratractis hystrix Reptiles (Freshwater turtle) Neotropical Sarmiento (1959)
Nouvelnema Nouvelnema cyclophoron Mammals Palaearctic Petter (1959)
Klossinemella Klossinemella iheringi Fish and reptiles Neotropical Costa (1961)
Pseudatractis Pseudatractis testudinicola Reptiles (Freshwater turtle) Oriental Yamaguti (1961)
Fitzsimmonsnema Fitzsimmonsnema reptiliae Reptiles (Tortoise) Ethiopian Petter (1966)
Orientatractis Orientatractis levanhoai Fish, amphibians and reptiles (Freshwater turtle and tortoise) Neotropical, Oriental, Ethiopian and Australian Petter (1966)
Pseudocyrtosomum Pseudocyrtosomum lucknowensis Reptiles (Freshwater turtle) Oriental Gupta and Johri (1987)
Buckleyatractis Buckleyatractis marinkelli Reptiles (Freshwater turtle) Neotropical Khalil and Gibbons (1988)
Podocnematractis Podocnematractis ortleppi Reptiles (Freshwater turtle) Neotropical Gibbons et al. (1995)
Diceronema Diceronema versterae Mammals Neotropical Gibbons et al. (1996)
Paraorientatractis Paraorientatractis semiannulata Reptiles (Freshwater turtle) Neotropical Gibbons et al. (1997)
Rhinoclemmysnema Rhinoclemmysnema multilabiatum Reptiles (Freshwater turtle) Neotropical Gibbons and Platt (2006)
Pneumoatractis Pneumoatractis podocnemis Reptiles (Freshwater turtle) Neotropical Bursey et al. (2009)
Rhinoceronema Rhinoceronema unicornensis Mammals Oriental Mondal and Manna (2013)
Hippopotamenema Hippopotamenema aliporensis Mammals Oriental Mondal and Manna (2015)
Vogtnema Vogtnema asymmetrica Reptiles (Freshwater turtle) Neotropical Jesus et al. (2022)
Open in a new tab

We assign the specimens described here to Atractidae because the esophagus is divided into two distinct portions: an anterior, cylindrical portion (corpus) and a posterior, elongated portion (isthmus) ending in a bulb. Males lack a precloacal sucker in the caudal region and possess two unequal spicules. Females are monodelphic and ovoviviparous, with the vulva located in the posterior region of the body, near the anus (Anderson et al., 2009).

The number and morphology of lips and the presence/absence of sclerotized structures such as spines and hooks are the main characteristics that differentiate genera within the Atractidae (Jesus et al., 2022). Based on these characteristics, Atractidae can be divided into two groups of species; the first group comprises genera whose lips have associated sclerotized structures (hooks and/or spines), including Klossinemella, Orientatractis, Crossocephalus, Paraorientatractis, Cobboldina, and Grassenema. The second group includes genera without sclerotized structures at the cephalic end, namely Nouvelnema, with the oral opening surrounded by two lips, Buckleyatractis, Labiduris, Paratractis, Pneumoatractis, and Pseudocyrtosomum with three lips; Cyrtosomum, Fitzsimmonsnema, Leiperenia, Monhysterides, Podocnematractis, Probstmayria, Pseudatractis, Rhinoceronema, and Rhinoclemmysnema, which have six lips; Vogtnema with four lips; and Hippopotamenema has the oral opening directed ventrally and lacks lips. Thus, Acanthoatractis n. gen., n. sp. belongs to the first group of genera in which the oral aperture has sclerotized structures.

Acanthoatractis n. gen. has eight wrench-shaped sclerotized structures around the mouth. Klossinemella and Orientatractis differ from the new genus by the number and shape of sclerotized structures around the mouth. Klossinemella has an oral opening surrounded by two bilobed formations (dorsal and ventral) resembling lips, with eight Y-shaped sclerotized structures, two subdorsal pairs, two laterodorsal pairs, two subventral pairs, and two lateroventral pairs. Additionally, a single horn is present between each subventral pair, and every two pairs have two small sublateral processes resembling papillae, sclerotized and oriented posteriorly to the amphids. Orientatractis species have six lips; each submedian lip has a well-sclerotized, recurved, pointed, bicornate chitinous piece and a single median spine. Furthermore, all species of Klossinemella and Orientatractis have a gubernaculum (Moravec and Thatcher, 1997; Jesus et al., 2023), whereas Acanthoatractis n. gen. lacks a gubernaculum.

The new genus lacks papillae at the cephalic end, and the oral opening has two sclerotized pieces, each with a pair of median hooks (one dorsal and one ventral). Crossocephalus, described in equines and rhinoceros, can be easily distinguished from the new genus Acanthoatractis by its numerous papillae at the cephalic end. Moreover, Crossocephalus has three lips (one dorsal and two submedian), each lip with a pair of hooks, and the anterior end of the esophagus with three pairs of eversible pectinate blades. The excretory pore is post-bulbar, and the esophageal bulb has valves (Berenger, 1947; York and Southwell, 1920), while in Acanthoatractis n. gen. the excretory pore is pre-bulbar, and the esophageal bulb does not have valves.

In Acanthoatractis n. gen., lips are absent, displaying eight pairs of spines (two subdorsal pairs, two dorsolateral pairs, two subventral pairs, and two ventrolateral pairs), and spines are absent posterior to the amphid pores. In contrast, Paraorientatractis from freshwater turtles has an oral opening with four submedian lips, each lip bearing a pair of recurved spines fused at the base and a single median spine near the distal margin, along with a pair of smaller spines posterior to the amphids. Additionally, Paraorientatractis has cuticular projections along the dorsal surface of the body (Gibbons et al., 1997), while Acanthoatractis n. gen. has a smooth cuticle.

Cobboldina found in hippopotami (Mammalia: Hippopotamidae), has a mouth surrounded by a cuticular sheath with a triangular median extension in dorsal and ventral positions (Leiper, 1911; Mondal and Manna, 2012) and differs from the new genus by the absence of hooks or spines in the mouth.

Finally, the new taxon differs by having the cephalic end surrounded by 16 pairs of spines distributed in a circle in subdorsal, dorsolateral, subventral, and ventrolateral positions. Grassenema, described in hiracoids (Mammalia: Hyracoidea), has the cephalic end surrounded by 12 pairs of cuticular spines arranged in two circles: the anterior circle with four pairs in subdorsal and subventral positions, and the posterior circle with eight pairs in subdorsal, subventral, and sublateral positions. Additionally, Grassenema possesses a buccal capsule and pharynx (Saito et al., 2021), structures that are absent in Acanthoatractis n. gen.

Thus, based on these morphological characters, the nematodes described here represent the 27th genus among atractids and the seventh report of this family in the P. unifilis species.

Ethics approval

We followed all applicable institutional, national, and international guidelines for animal care and use. The study is registered with the Animal Ethics Committee from the UFPA under code 8341260821. The present study was approved by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), Brazil, and host specimens were collected under license number SISBIO: 53527-4.

Funding

This study was supported by Coordination for the Improvement of High Higher Education Personnel (CAPES)/Postgraduate Program in the Biology of Infectious and Parasitic Agents (PPGBAIP)/UFPa, Amazon Foundation for Research and Studies Support (FAPESPA), Programa de Apoio a Nucleos Emergentes (FAPESPA/CNPq PRONEM 01/2021, process number 51/2021); Research productivity scholarship of CNPq to F.T.V. Melo (Process number 314116/2021-4). This study is part of the Ph.D. thesis of Ronald Ferreira de Jesus in PPGBAIP (Institute of Biological Sciences-UFPa).

CRediT authorship contribution statement

Ronald Ferreira Jesus: Writing – review & editing, Writing – original draft, Software. Bianca Nandyara: Resources. Jeannie Nascimento dos Santos: Formal analysis. Francisco Tiago de Vasconcelos Melo: Writing – original draft, Supervision, Funding acquisition.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We are grateful to Ana Nunes Santos for her support in host necropsies and collection of nematodes; to Yuri Willkens for his technical support with SEM analyses and Dra. Edilene Oliveira da Silva, from Laboratory of Cellular Structural Biology at the Federal University of Pará, Belém, for her technical support with the SEM analyses.

References

  1. Amato J.F.R., Walter A.B., Amato S.B. In: Protocolo para Laboratório: Coleta e Processamento de Parasitas de Pescado. Universitária Impressa., editor. Universidade Federal Rural do Rio de Janeiro; Seropédica, Brasil: 1991. [Google Scholar]
  2. Anderson R.C., Chabaud A.G., Willmott S. vol. 2009. CABI; Wallingford: 2009. (Keys to the Nematode Parasites of Vertebrates: Archival Volume). [Google Scholar]
  3. Baylis H.A., Daubney R. Report on the parasitic nematodes in the collection of the Zoological Survey of India. Mem. Indian Mus. 1922;7:342–343. [Google Scholar]
  4. Berenger J.G. Revisión de la familia Atractidae Travassos, 1920 com descripción de dos nuevas especies. Rev. Iber. Parasitol. 1947;7:3–90. [Google Scholar]
  5. Bursey C.R., Reavill D., Greiner E. vol. 76. Comp Parasitol; 2009. pp. 149–153. (Pneumoatractis podocnemis n. gen., n. sp. (Nematoda: Atractidae) from the Yellow-Spotted Amazon River Turtle, Podocnemis unifilis (Testudines: Pelomedusidae)). [DOI] [Google Scholar]
  6. Costa S.C.G. Sobre a sistemática da família Cobboldinidae Skyardin, 1948 (Nematoda) Atas Soc. Biol. Rio de Janeiro. 1961;5:30–31. [Google Scholar]
  7. Dujardin M.F. 1845. Histoire naturelle des helminthes or vers intestinaux; p. 654. Paris, France. [Google Scholar]
  8. Ferrara C.R., Fagundes C.K., Morcatty T.Q., Vogt R.C. Wildlife Conservation Society. 2017. Quelônios Amazônicos: Guia de Identificação e Distribuição; pp. 1–182. Manaus. [Google Scholar]
  9. Gedoelst L. Un Oxyuridé nouveau parasite d'un reptile. Comptes Rendus SocietyBiology Paris. 1919;82:910–913. [Google Scholar]
  10. Gibbons L.M., Khalil L.F., Marinkelle C.J. New nematode genus, Podocnematractis, for Atractis ortleppi Thapar, 1925 (Cosmocercoidea: Atractidae) and the description of another new species, P. colombiaensis from turtles Podocnemis spp. in Colombia. Syst. Parasitol. 1995;30:47–56. doi: 10.1007/BF00009244. [DOI] [Google Scholar]
  11. Gibbons L.M., Knapp S.E., Krecek R.C. Diceronema versterae gen. n., sp. n. (Atractidae; Cosmocercoidea) from the Black Rhinoceros, Diceros bicornis bicornis, in South Africa. J Helminthol Soc Wash. 1996;63:98–104. [Google Scholar]
  12. Gibbons L.M., Khalil L.F., Marinkelle C.J. vol. 92. Mem Ins Oswaldo Cruz; 1997. pp. 359–364. (Paraorientatractis semiannulata n. g., n. sp. (Cosmocercoidea: Atractidae) from the Large Intestine of the Side-Necked Turtle, Podocnemis unifilis Troschel, 1848 (Testudines: Pelomedusidae) in Brazil). [DOI] [PubMed] [Google Scholar]
  13. Gibbons M.L., Platt T.R. Rhinoclemmysnema n. g. and three new species of nematodes of the family Atractidae (Cosmocercoidea), with notes on the helminth fauna of Rhinoclemmys pulcherrima (Testudines: Bataguridae) in Costa Rica. J. Helminthol. 2006;80:333–340. doi: 10.1017/joh2006360. [DOI] [PubMed] [Google Scholar]
  14. Gupta V., Johri S. On a new genus Pseudocyrtosomum (Atractidae: Nematoda) from Kachuga dhongoka gray from lucknow. Indian J. Helminthol. 1987;39:83–87. [Google Scholar]
  15. ICZN International commission on zoological nomenclature: amendment of articles 8, 9, 10, 21 and 78 of the international code of zoological nomenclature to expand and refine methods of publication. Zootaxa. 2012;3450:1–7. doi: 10.3897/zookeys.219.3994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jesus R.F., Cardoso E.L., Willkens Y., Furtado A.P., Santos J.N., Melo F.T.V. “Long time no see”: redescription of Orientatractis leiperi (Nematoda: Atractidae) parasite of Podocnemis unifilis (Testudines: Podocnemididae) from Pará state, Brazil. Rev. Mex. Biodivi. 2020;91:1–7. doi: 10.22201/ib.20078706e.2020.91.3464. [DOI] [Google Scholar]
  17. Jesus R.F., Santos A.N., Nandyara B., Santos J.N., Melo F.T.V. Vogtnema asymmetrica n. gen., n. sp. (Nematoda: Cosmocercoidea: Atractidae) parasite of Rhinoclemmys punctularia (Daudin) (Testudines: Geoemydidae) from eastern Amazon. Syst. Parasitol. 2022;99:761–769. doi: 10.1007/s11230-022-10065-1. Brazil. [DOI] [PubMed] [Google Scholar]
  18. Jesus R.F., Oliveira S.C.G., Ramos I.M.C., Melo F.T.V. A new species of Orientatractis (Nematoda: Cosmocercoidea: Atractidae) parasite of yellow-spotted Amazon river turtle, Podocnemis unifilis Troschel, 1848 (Testudines: Podocnemididae) in Brazilian Amazon. Int J Parasitol Parasites Wildl. 2023;22:108–112. doi: 10.1016/j.ijppaw.2023.09.006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Khalil L.F., Gibbons L.M. Two nematodes, Paratractis hystrix (Diesing, 1851) and Buckleyatractis marinkelli n. g., n. sp. (Atractidae: Cosmocercoidea) from Podocnemis spp. in Colombia. Syst. Parasitol. 1988;12:187–198. doi: 10.1007/BF00007767. [DOI] [Google Scholar]
  20. Khalil M. A preliminary note on some new nematode parasites from the elephant. Ann. Mag. Nat. Hist. 1922;9:212–216. doi: 10.1080/00222932208632662. [DOI] [Google Scholar]
  21. Leiper T. Some new parasitic nematodes from tropical Africa. Proc. Zool. Soc. Lond. 1911;12:549–555. [Google Scholar]
  22. Mondal S., Manna B. On a new species of the genus Cobboldina (Nematoda: Atractidae) from Hippopotamus (Hippopotamus amphibius Linnaeus, 1758) captivated at the alipore zoological garden, Kolkata, West Bengal, India. Indian Soc Parasitol. 2012;36:251–255. doi: 10.1007/s12639-012-0118-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mondal S., Manna B. Rhinoceronema unicornensis gen. n., sp. n. (Cosmocercoidea: Atractidae) from Indian one horned rhinoceros (Rhinoceros unicornis Linnaeus, 1758) captivated at the alipore zoological garden, Kolkata, India. J. Parasit. Dis. 2013;37:134–141. doi: 10.1007/s12639-012-0147-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mondal S., Manna B. Hippopotamenema aliporensis gen. n. sp. n. (Nematoda: Atractidae) from Hippopotamus (Hippopotamus amphibius Linnaeus, 1758) captivated at the alipore zoological garden, Kolkata, West Bengal, India. Sci. Cult. 2015;81:44–47. doi: 10.1007/s12639-012-0118-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Moravec F., Thatcher V.E. New data on the morphology and systematic status of Klossinemella iheringi (Nematoda: Atractidae) from Amazonian serrasalmid fish. Folia Parasitol. 1997;44:48–54. [Google Scholar]
  26. Petter A.J. Deux nouveaux genres de nematodes atractides, parasites du daman des rochers (Procavia ruficeps) (Ehrenberg) Bull Soc Zool. 1959;84:195–204. [Google Scholar]
  27. Petter A.J. Équilibre des espèces dans les populations de nématodes parasites du colon des tortues terrestres. Mémoires du Muséum National d’Histoire Naturelle, Paris, Serie Zoologie. 1966;39:1–245. [Google Scholar]
  28. Railliet A. Probstmayria vivipara, nèmatode du cheval. Recueil de Médecine Véterinaire. Paris. 1909;86:336. [Google Scholar]
  29. Ransom B.H. Probstmayria vivipara (Probstmayr, 1865) Ransom, 1907, a nematode of horses heretofore unreported from the United States. Trans. Am. Microsc. Soc. 1907;27:33–41. doi: 10.2307/3220886. [DOI] [Google Scholar]
  30. Saito T., Hayashi K., Hayashi K., Akita Y., Une Y., Kuroki T., Shibahara T., Takashima Y. Morphological observation and first molecular characterization of Grassenema procaviae Petter, 1959 (Cosmocercoidea: Atractidae) in the stomach of Cape hyrax (Procavia capensis) raised in a zoo in Japan. Parasitol. Int. 2021;84 doi: 10.1016/j.parint.2021.102385. [DOI] [PubMed] [Google Scholar]
  31. Sarmiento L. Description of Paratractis hystrix (Diesing, 1851) gen. nov. (Nematoda: Atractidae) from Podocnemis dumeriliana. J. Parasitol. 1959;45:65–68. doi: 10.2307/3274788. [DOI] [PubMed] [Google Scholar]
  32. Schneider A. G. Reimer; Berlin, Germany: 1866. Monographie Der Nematoden; pp. 1–357. [Google Scholar]
  33. Travassos L. Esboço de uma chave geral dos nematodes parasitos. Rev. Vet. Zoot. Rio de Janeiro. 1920;10:59–71. [Google Scholar]
  34. York W., Southwell T. Crossocephalus zebrae, n. sp. Ann. Trop. Med. Parasitol. 1920;14:127–135. doi: 10.1080/00034983.1920.11684226. [DOI] [Google Scholar]
  35. Yamaguti S. Interscience Publishers; New York: 1961. Systema Helminthum. Volume III. The Nematodes of Veterbrates; pp. 134–135. [Google Scholar]

Articles from International Journal for Parasitology: Parasites and Wildlife are provided here courtesy of Elsevier

RESOURCES