New species of Polystomoides (Monogenoidea: Polystomatidae) parasitizing the urinary bladder of a freshwater turtle in Brazil

Nova espécie de Polystomoides (Monogenoidea: Polystomatidae) parasitando a bexiga urinária de uma tartaruga de água doce no Brasil

Abstract

Trachemys dorbigni is the most abundant freshwater turtle species in Rio Grande do Sul, southern Brazil. Chelonians are known to host a wide variety of pathogens, including viruses, bacteria, hemoparasites and helminths. Among these, nine genera of polystomatid flatworms (Monogenoidea; Polystomatidae) infect freshwater turtles: Apaloneotrema, Aussietrema, Fornixtrema, Manotrema, Pleurodirotrema, Polystomoidella, Polystomoides, Uropolystomoides and Uteropolystomoides. However, little is known about the biology of these parasites in the Neotropical Realm. Through investigative cystoscopy, specimens of Polystomatidae were located inside the urinary bladder of the host T. dorbigni. Retrieved specimens were fixed and stained whole mounts prepared for taxonomic identification. In the present paper, a new species of Polystomoides (Monogenoidea: Polystomatidae) parasitizing the urinary bladder of a freshwater turtle of the species T. dorbigni in Brazil is described. Polystomoides santamariensis n. sp. differs from the congeneric species on the length of the genital spines, which are longer. Given the enormous diversity of freshwater turtles around the world, it is likely that a large number of chelonian polystomatids are still unknown.

Keywords:
Platyhelminthes; chelonians; Rio Grande do Sul; Trachemys dorbigni

Resumo

Trachemys dorbigni é a espécie de tartaruga de água doce mais abundante do Rio Grande do Sul, no Sul do Brasil. Sabe-se que os quelônios são hospedeiros de uma grande variedade de patógenos, incluindo vírus, bactérias, hemoparasitos e helmintos. Dentre estes, oito gêneros de Polystomatidae (Platyhelminthes: Monogenoidea) infectam tartarugas de água doce: Apaloneotrema, Aussietrema, Fornixtrema, Manotrema, Pleurodirotrema, Polystomoidella, Polystomoides, Uropolystomoides e Uteropolystomoides. No entanto, pouco ainda se sabe sobre a biologia destes parasitos na Região Neotropical. Durante uma citoscopia investigativa, foram observados espécimes de Polystomatidae localizados no interior da bexiga urinária de T. dorbigni. Os espécimes coletados foram fixados e corados para identificação taxonômica. No presente artigo, uma nova espécie de Polystomoides (Monogenoidea: Polystomatidae) parasitando a bexiga urinária de tartaruga de água doce da espécie T. dorbigni no Brasil é descrita. Polystomoides santamariensis n. sp. difere das demais espécies no tamanho dos espinhos genitais, que são maiores. Devido a enorme diversidade de tartarugas de água doce ao redor do mundo, é provável que um grande número de polistomatídeos de quelônios ainda seja desconhecido.

Palavras-chave:
Platelmintos; quelônios; Rio Grande do Sul; Trachemys dorbigni

Introduction

With 795 of the 11,733 known reptiles species of the world from Brazil, it is the country with the third-largest diversity of reptiles (Costa & Bérnils, 2018; Uetz et al., 2023). The order Testudines comprises turtles, tortoises and terrapins (freshwater turtles) and is composed of two suborders: Pleurodira and Cryptodira. The first has distribution only in the southern hemisphere, across the Australian, Ethiopian and Neotropical Realms, while Cryptodira has the largest number of living species, with distribution on all continents, with the exception of Australia and Antarctica (Van Dijk et al., 2014; Rhodin et al., 2021; Du Preez et al., 2022). In Brazil, 36 species of Testudines have been described (Costa & Bérnils, 2018) and in the state of Rio Grande do Sul, there are 11 chelonian species, among which five are marine and six are freshwater species (Lema & Ferreira, 1990). Among the latter, Trachemys dorbigni Duméril & Bibron, 1835, is the most abundant (Bujes et al., 2011). In Brazil, it occurs naturally in Rio Grande do Sul and Santa Catarina, and it also inhabits other countries such as Argentina and Uruguay (Rhodin et al., 2021).

Species of Trachemys Agassiz, 1857 present the widest geographical distribution among New World chelonians, such that their range extends from the United States to Argentina (Seidel, 2002). This genus comprises 15 species and, in addition to Trachemys dorbigni, in South America Trachemys callirostris Gray, 1856, is found in Colombia and Venezuela and Trachemys adiutrix Vanzolini, 1995, in Brazil (Van Dijk et al., 2014).

Freshwater turtles are known to host a wide variety of pathogens that belong to all major groups of parasites (e.g. viruses, bacteria, hemoparasites and helminths). Among these, Polystomatidae (Platyhelminthes: Monogenoidea) is the largest family of monogenoideans and comprises 32 genera, among which Apaloneotrema Du Preez & Verneau, 2020, Aussietrema Du Preez & Verneau, 2020, Fornixtrema Du Preez & Verneau, 2020, Manotrema Du Preez, Domingues & Verneau, 2022, Pleurodirotrema Du Preez, Domingues & Verneau, 2022, Polystomoidella Price, 1939, Polystomoides Ward, 1917, Uropolystomoides Tinsley & Tinsley, 2016 and Uteropolystomoides Tinsley, 2017 infect freshwater turtles (Morrison & Du Preez, 2011; Chaabane et al., 2022; Du Preez et al., 2022).

At present from the Neotropical realm three species are known from the conjunctival sacs of their chelonian hosts namely Fornixtrema fentoni (Platt, 2000) from Kinosternon leucostomum (Duméril & Duméril, 1851) and Rhinoclemmys pulcherrima (Gray, 1856), Fornixtrema guianense (Du Preez et al., 2017) from Rhinoclemmys punctularia (Daudin, 1801) and Fornixtrema scorpioides (Du Preez et al., 2017) from Kinosternon scorpioides (Linnaeus, 1766).

From the oral region of their chelonian hosts currently are known Manotrema brasiliensis (Vieira et al., 2008) from Hydromedusa maximiliani (Mikan, 1820) and Phrynops geoffroanus (Schweigger, 1814), Manotrema fuquesi (Mané-Garzon & Gil, 1962) and Manotrema uruguayensis (Mané-Garzon & Gil, 1961) from Phrynops hilarii (Duméril & Bibron, 1835), Polystomoides magdalenensis Lenis & Garcia-Prieto, 2009 from Trachemys callirostris callirostris (Gray, 1856) and Polystomoides rohdei Mané-Garzon & Holcman-Spector, 1968 from Trachemys dorbigni (=Pseudemys dorbigni).

From the urinary bladder of their chelonian hosts are known Polystomoides cayensis (Du Preez et al., 2017) from Rhinoclemmys punctularia and Polystomoides domitilae (Caballero, 1938) Price, 1939 from Chrysemys ornata (= Trachemys scripta ornata).

Through investigative cystoscopy after video-assisted ovariosalpingectomy performed on an individual of the species T. dorbigni, specimens of Polystomatidae were found. In the present paper, a new species of Polystomoides (Monogenoidea: Polystomatidae) parasitizing the urinary bladder of this freshwater turtle in Brazil is described.

Material and Methods

One specimen of T. dorbigni (D'Orbigny's slider or “Tartaruga-tigre-d'agua”) was subjected to investigative cystoscopy after video-assisted ovariosalpingectomy in the Veterinary Hospital of the Federal University of Santa Maria (UFSM). This animal came from the São Braz conservation breeding station (“Criadouro Conservacionista São Braz”), located in Santa Maria, Rio Grande do Sul, Brazil (29º 41′ 03” S; 53º 48′ 25” W). Elective castration was performed on this individual as a population control measure.

During the cystoscopy, using a 30° scope Karl Storz^TM, Tuttlingen, Germany (1.9-2.0 mm) inside in a working sheath (9.6 Fr.) and semi-rigid forceps (Karl Storz^TM, Tuttlingen, Germany), three helminth specimens that were found attached to the urinary bladder were collected. These were sent to the Veterinary Parasitology Laboratory of UFSM for identification at the species level, and subsequently to the Laboratory for Helminth Parasites of Fish, Oswaldo Cruz Institute, Oswaldo Cruz Foundation. The samples were fixed in 70% alcohol and stored. Specimens were stained with Langeron’s alcoholic acid carmine, dehydrated in an ethyl alcohol series, cleared in beechwood creosote and mounted in Canada balsam as permanent slides (Eiras et al., 2006). Measurements are presented in micrometers, unless otherwise stated, as range values followed by mean values, when more than two, and the number of structures measured, where applicable, in parentheses. Specimens were illustrated with the aid of a camera lucida coupled to a Zeiss Axioskop light microscope. Light microphotographs were made with the use of the ZEN 2 software (Blue edition) ^®; Carl Zeiss Microscopy, 2011. The authorship of the taxa followed the recommendation of Article 50.1 of the International Code of Zoological Nomenclature (ICZN), which deals with the identity of the authors. The holotype and paratypes were deposited in the Helminthological Collection of the Oswaldo Cruz Institute (“Coleção Helmintológica do Instituto Oswaldo Cruz”, CHIOC), Rio de Janeiro, Brazil.

Results

Class Monogenoidea Bychowsky, 1937

Order Polystomatidea Lebedev, 1988

Family Polystomatidae Gamble, 1896

Polystomoides Ward, 1917

Polystomoides santamariensis Lignon, Cohen, Justo, Du Preez & Monteiro n. sp. (Figures 1-3)

Figure 1
Polystomoides santamariensis n. sp. Holotype. A - Ventral view. Bar= 1mm; B - Genital spines. Bar= 100 μm; C - Marginal hooklets. Bar= 10 μm. Abbreviations: mo, mouth; ph, pharynx; gb, genital bulb; vd, vas deferens; eg, egg; va, vagina; ov, ovary; ic, intestinal cecum; te, testis; su, sucker; hp, haptor.

Figure 3
Specimens of Polystomoides santamariensis n. sp. in host’s urinary bladder (Trachemys dorbigni). A - Parasite fixed in mucosa (arrow); B - View of its suckers; C - Parasite stretching to move; D - Specimen collected using semi-rigid forceps.

Host:Trachemys dorbigni (Duméril & Bibron, 1835) (adult female)

Site: Urinary bladder

Locality: Santa Maria, Rio Grande do Sul, Brazil (29º 41′ 03” S; 53º 48′ 25” W).

Type-material: Holotype CHIOC 39994 a, Paratypes CHIOC 39994 b, c.

Etymology: The specific name refers to the locality, Santa Maria.

Description (based on 3 sexually mature specimens stained with acid carmine): Body elongated and ellipsoid, 3,000-4,350 (3,742) long by 1,500-1,675 (1,600) wide and 1,400 at vaginae level (Figures 1A, 2A, 3A). Mouth subterminal, surrounded by a false oral sucker, 410-470 (443) long by 410-450 (423) wide; Pharynx muscular, subspherical, 235-265 (255) long by 295-330 (310) wide (Figures 1A, 2A, B); esophagus short and intestine bifurcates into two intestinal caeca, non-confluent posteriorly to gonads, lacking diverticula, extending to posterior region of trunk, not reaching the haptor region. Intercaecal gonads, testis posterior to ovary. Testis single, spherical with poorly developed lobes, mid-ventral, posterior to ovary, 530-600 (560) long by 610-700 (643) wide. Seminal vesicle a dilatation of vas deferens, sigmoid, crossing midline, followed by genital bulb (Figures 1A, 2A). Genital bulb 155 and 175 long by 160 and 200 wide, presenting 16 genital spines, 37-42 (40; n = 8) long (Figures 1B, 2C). Ovary sinistral, elongated, 240 and 320 long by 100 and 110 wide. Two vaginae present, located marginally, at level of middle of body proper, intervaginal distance of 85.7% of the body width at the level of the vaginae, located at 1,200 and 1,600 from the anterior extremity (Figures 1A, 2A). Haptor 1,250-1,400 (1,325) long by 1,250-1,675 (1,508) wide. Six haptoral suckers, cup-shaped with elaborate skeletal elements, 225-440 (412; n = 18) long by 315-465 (349; n = 18) wide (Figures 1A, 2A, 3B). Egg 250 and 275 long by 200 and 275 wide. Hamuli absent. Marginal hooklets 13-15 (14; n = 3) long retained in adult parasites, similar in size and shape (Figure 1C).

Figure 2
Polystomoides santamariensis n. sp. A - Total, ventral view. Bar= 1mm; B - Anterior region, showing mouth and pharynx. Bar= 300 μm; C - Genital bulb with 16 spines. Bar= 100 μm.

Remarks

The new species is similar to Polystomoides species previously assigned to Neopolystoma, considering the absence of hamuli: P. aspidonectis (MacCallum, 1918), P. cayensis (Du Preez et al., 2017), P. cyclovitellum (Caballero et al., 1956), P. domitilae (Caballero, 1938), P. euzeti (Combes & Ktari, 1976), P. exhamatum (Ozaki, 1935), P. orbiculare (Stunkard, 1916), P. rugosa (MacCallum, 1918), and P. terrapenis (Harwood, 1932).

The new species is similar to P. cyclovitellum, P. exhamatum, P. orbiculare, P. terrapenis and P. cayensis, in terms of the number of spines in the genital atrium. Polystomoides santamariensis n. sp. differs from these congeneric species on the length of the genital spines, which are longer (Stunkard, 1916; Harwood, 1932; Ozaki, 1935; Price, 1939; Caballero et al., 1956; Lamothe-Argumedo, 1972; Du Preez et al., 2017). Besides, regarding the number of genital atrium spines and absence of hamuli, it resembles Fornixtrema fentoni (Platt, 2000), Fornixtrema guianensis (Du Preez et al., 2017), Fornixtrema scorpioides (Du Preez et al., 2017), and Pleurodirotrema chelodinae (MacCallum, 1918), species previously allocated in Neopolystoma, differing also from the size of genital spines.

According to Du Preez et al. (2022), the inter-vaginal distance that corresponds to Polystomoides infecting cryptodires ranges from 84.2-99.4% and the intervaginal distance observed in P. santamariensis fits this range. Nonetheless, these authors stated that the number of genital spines for Polystomoides infecting cryptodires ranges from 24 to 44, which is not in agreement to the number presented in the specimens described herein.

Du Preez & Theunissen (2021) proposed four types of haptoral suckers for polystomes. Their Type III corresponds to Type 2 of Pichelin (1995) and is the type present in all polystomes infecting chelonian hosts. These suckers are spherical, symmetrical, firm, directed ventrolaterally and characterized by having embedded skeletal elements that provide a secure grip on the host tissue. The morphology of the haptoral suckers of Polystomoides santamariensis n. sp. is in agreement with type III proposed by these authors.

Discussion

Polystomoides was originally described as a sugbgenus of Polystoma Zeder, 1800 by Ward (1917), based on the presence of a short ovary with a single egg, being elevated to genus rank by Ozaki (1935) who pointed to the absence of a uterus as a diagnostic character (Chaabane et al., 2022). Species of the genus are found in the mouth, esophagus, nasal cavities and urinary bladder of turtles and had been charaterized by the presence of two pairs of hamuli in the haptor (Vieira et al., 2008; Chaabane et al., 2022). Price (1939) proposed two new genera for polystomatids of chelonians: Polystomoidella Price, 1939 parasites of the urinary bladder of their hosts and Neopolystoma Price, 1939 found in the urinary bladder and nasal cavities, differing in the absence and number of hamuli, Polystomoides spp. have 2 pair of hamuli, Polystomoidella spp. have 1 pair and Neopolystoma spp. none (Vieira et al., 2008; Du Preez & Van Rooyen, 2015; Du Preez & Verneau, 2020; Chaabane et al., 2022). Only recently, the polystomatid genera parasitizing chelonians received considerable attention, with the description of Uropolystomoides; Uteropolystomoides; Aussietrema; Fornixtrema; Apaloneotrema; Manotrema and Pleurodirotrema; and the synonymizing of Neopolystoma to a junior synonym of Polystomoides [see Tinsley (2017); Tinsley & Tinsley (2016); Du Preez & Verneau (2020); Du Preez et al. (2022)]. Some species previously allocated in Polystomoides were transferred to Uropolystomoides, Uteropolystomoides, and Manotrema based in one or more characteristics (Du Preez et al., 2022; Price, 1939; Tinsley, 2017; Tinsley & Tinsley, 2016). All the South American species of Polystomoides infecting the oral region Pleurodira freshwater turtles were transferred to Manotrema: Manotrema uruguayensis (Mané-Garzón & Gil, 1961), Manotrema fuquesi (Mané-Garzón & Gil, 1962) and Manotrema brasiliensis (Vieira et al., 2008) (Du Preez et al., 2022).

Chaabane et al. (2022) proposed the name Polystomoides for the clade composed by Neopolystoma and Polystomoides, considering the similarity in the morphology of the vaginae, reassigning nine species, previously attributed to Neopolystoma, for Polystomoides, and redefined the genus as polystomes species infecting oral cavity and urinary bladder of cryptodires, presenting or not hamuli and peripheral vaginae. Based on its unique morphology they retained Uteropolystomoides although it shares the same clade (Chaabane et al., 2022). Considering this proposition, the new species is allocated in Polystomoides, being the first species of the genus described in Brazil.

Considering the recent studies regarding the taxonomy of the polystomes parasites of turtles, further molecular studies are needed to clarify the phylogenetic relationships of these genera, to be compared to morphological and biological findings. Polystomes are grouped mainly by the site of infection considering that they present site specificity, which can lead to the process of speciation and explain the diversity of parasite species found in freshwater turtles (Du Preez & Van Rooyen, 2015). Given the enormous diversity of freshwater turtles around the world, it is likely that a large number of chelonian polystomatids are still unknown.

The present paper highlighted the value of non-invasive and non-lethal procedures to investigate the polystomatid fauna since the specimens were collected during surgery.

Acknowledgements

This study was supported financially by the Brazilian Coordination Office for Higher-Education Personnel Training (CAPES) and the National Council for Scientific and Technological Development (CNPq). MVB was supported through the CNPq/Productivity in Research (3304353/2021-3) program.

• How to cite: Lignon JS, Cohen SC, Justo MCN, Du Preez L, Comarella CG, Nishimaru RA, et al. New species of Polystomoides (Monogenoidea: Polystomatidae) parasitizing the urinary bladder of a freshwater turtle in Brazil. Braz J Vet Parasitol 2023; 32(3): e007823. https://doi.org/10.1590/S1984-29612023045

References

• Bujes CS, Molina FB, Verrastro L. Population characteristics of Trachemys dorbigni (Testudines, Emydidae) from Delta do Jacuí State Park, Rio Grande do Sul, Southern Brazil. South Am J Herpetol 2011; 6(1): 27-34. http://dx.doi.org/10.2994/057.006.0104
  » http://dx.doi.org/10.2994/057.006.0104
• Caballero E, Zerecero MC, Grocott RG. Helmintos de la Republica de Panama. XIX. Algunos trematodos de quelonios de agua dulce. An Inst Biol Mex 1956; 27: 415-430.
• Chaabane A, Du Preez L, Johnston G, Verneau O. Revision of the systematics of the Polystomoidinae (Platyhelminthes, Monogenea, Polystomatidae) with redefinition of Polystomoides Ward, 1917 and Uteropolystomoides Tinsley, 2017. Parasite 2022; 29: 56. http://dx.doi.org/10.1051/parasite/2022056 PMid:36562437.
  » http://dx.doi.org/10.1051/parasite/2022056
• Costa HC, Bérnils RS. Répteis do Brasil e suas Unidades Federativas: lista de espécies. Herpetol Bras 2018; 7(1): 11-57.
• Du Preez LH, Badets M, Héritier L, Verneau O. Tracking platyhelminth parasite diversity from freshwater turtles in French Guiana: First report of Neopolystoma Price, 1939 (Monogenea: Polystomatidae) with the description of three new species. Parasit Vectors 2017; 10(1): 53. http://dx.doi.org/10.1186/s13071-017-1986-y PMid:28143592.
  » http://dx.doi.org/10.1186/s13071-017-1986-y
• Du Preez LH, Domingues MV, Verneau O. Classification of pleurodire polystomes (Platyhelminthes, Monogenea, Polystomatidae) revisited with the description of two new genera from the Australian and Neotropical Realms. Int J Parasitol Parasites Wildl 2022; 19: 180-186. http://dx.doi.org/10.1016/j.ijppaw.2022.09.004 PMid:36188110.
  » http://dx.doi.org/10.1016/j.ijppaw.2022.09.004
• Du Preez LH, Theunissen M. A sucker for the job: morphology and functioning of suckers of polystomatid monogeneans. Folia Parasitol 2021; 68(006): 1-10. http://dx.doi.org/10.14411/fp.2021.006 PMid:33843655.
  » http://dx.doi.org/10.14411/fp.2021.006
• Du Preez LH, Van Rooyen M. A new polystomatid (Monogenea, Polystomatidae) from the mouth of the North American freshwater turtle Pseudemys nelsoni. ZooKeys 2015; 539(539): 1-9. http://dx.doi.org/10.3897/zookeys.539.6108 PMid:26798243.
  » http://dx.doi.org/10.3897/zookeys.539.6108
• Du Preez LH, Verneau O. Eye to eye: classification of conjunctival sac polystomes (Monogenea: Polystomatidae) revisited with the description of three new genera Apaloneotrema n. g., Aussietrema n. g. and Fornixtrema n. g. Parasitol Res 2020; 119(12): 4017-4031. http://dx.doi.org/10.1007/s00436-020-06888-w PMid:33043418.
  » http://dx.doi.org/10.1007/s00436-020-06888-w
• Eiras JC, Takemoto RM, Pavanelli GC. Métodos de estudo e técnicas laboratoriais em parasitologia de peixes 2nd ed. Maringá: Eduem; 2006.
• Harwood PD. The helmiths parasitic in the amphibia and reptilia of Houston, Texas and vicinity. Proc U S Natl Mus 1932; 81(2940): 1-71. http://dx.doi.org/10.5479/si.00963801.81-2940.1
  » http://dx.doi.org/10.5479/si.00963801.81-2940.1
• Lamothe-Argumedo R. Monogeneos de reptiles I. Redescripción de cuatro especies de Monogenea (Polystomatidae) parásitos de la vejiga urinaria de tortugas de Mexico. An Inst Biol Univ Nac Autón México 1972; 43: 1-16.
• Lema T, Ferreira MTS. Contribuição ao conhecimento dos testudines do Rio Grande do Sul (Brasil). Lista sistemática comentada (Reptilia). Acta Biol Leopoldensia 1990; 12(1): 125-164.
• Morrison C, Du Preez LH. Turtle polystomes of the world: Neopolystoma, Polystomoidella & Polystomoides Saarbrücken: VDM Verlag Dr. Müller; 2011.
• Ozaki Y. Studies on the frog - trematode Diplorchis ranae I. Morphology of the adult form with review of the family Polystomatidae. J Sci Hiroshima Univ 1935; 3: 193-223.
• Pichelin S. Parapolystoma johnstoni n. sp. from Litoria nyakalensis (Amphibia) in Australia and taxonomic considerations on the Diplorchiinae (Monogenea). J Parasitol 1995; 81(2): 261-265. http://dx.doi.org/10.2307/3283931 PMid:7707205.
  » http://dx.doi.org/10.2307/3283931
• Price EW. North American monogenetic trematodes. IV. The family Polystomatidae (Polystomatoidea). Proc Helminthol Soc Wash 1939; 6(2): 80-92.
• Rhodin AGJ, Iverson JB, Bour R, Fritz U, Georges A, Shaffer HB, et al. Turtles of the world: annotated checklist and atlas of taxonomy, synonymy, distribution, and conservation status 9th ed. Arlington: Chelonian Research Foundation; Ojai: Turtle Conservancy; 2021. http://dx.doi.org/10.3854/crm.8.checklist.atlas.v9.2021
  » http://dx.doi.org/10.3854/crm.8.checklist.atlas.v9.2021
• Seidel ME. Taxonomic observations on extant species and subspecies of slider turtles, genus Trachemys. J Herpetol 2002; 36(2): 285-292. http://dx.doi.org/10.1670/0022-1511(2002)036[0285:TOOESA]2.0.CO;2
  » http://dx.doi.org/10.1670/0022-1511(2002)036[0285:TOOESA]2.0.CO;2
• Stunkard HW. On the anatomy and relationships of some North American trematodes. J Parasitol 1916; 3(1): 21-27. http://dx.doi.org/10.2307/3270743
  » http://dx.doi.org/10.2307/3270743
• Tinsley RC, Tinsley MC. Tracing ancient evolutionary divergence in parasites. Parasitology 2016; 143(14): 1902-1916. http://dx.doi.org/10.1017/S0031182016001347 PMid:27576454.
  » http://dx.doi.org/10.1017/S0031182016001347
• Tinsley RC. Reproductive innovation and the recognition of a new genus within the Polystomatidae (Monogenea) infecting chelonian vertebrates. Folia Parasitol 2017; 64(017): 1-11. http://dx.doi.org/10.14411/fp.2017.017 PMid:28620151.
  » http://dx.doi.org/10.14411/fp.2017.017
• Uetz P, Freed P, Aguilar R, Hošek J. The reptile database [online]. Heidelberg: The Reptile Database; 2023 [cited 2023 Mar 5]. Available from: http://www.reptile-database.org
  » http://www.reptile-database.org
• Van Dijk PP, Iverson JB, Rhodin AGJ, Shaffer HB, Bour R. Turtles of the world 7th edition: annotated checklist of taxonomy, synonymy, distribution with maps, and conservation status. Chelon Research Monog 2014; 5: 329-479. http://dx.doi.org/10.3854/crm.5.000.checklist.v7.2014
  » http://dx.doi.org/10.3854/crm.5.000.checklist.v7.2014
• Vieira FM, Novelli IA, Sousa BM, Lima SS. A new species of Polystomoides Ward, 1917 (Monogenea: Polystomatidae) from freshwater chelonians (Testudines: Chelidae) in Brazil. J Parasitol 2008; 94(3): 626-630. http://dx.doi.org/10.1645/GE-1417R.1 PMid:18605799.
  » http://dx.doi.org/10.1645/GE-1417R.1
• Ward HB. On the structure and classification of North American parasitic worms. J Parasitol 1917; 4(1): 1-12. http://dx.doi.org/10.2307/3271103
  » http://dx.doi.org/10.2307/3271103

Publication Dates

• Publication in this collection
  24 July 2023
• Date of issue
  2023

History

• Received
  04 May 2023
• Accepted
  19 June 2023