Parapharyngodon hispidus n. sp. (Nematoda: Pharyngodonidae) in Tropidurus hispidus (Spix) (Squamata: Tropiduridae) from Caatinga Biome of the Vale do São Francisco, state of Pernambuco, Brazil with a key for the Neotropical species of the genus Parapharyngodon Chatterji Author Ferreira, Antonio Carlos Santos 0000-0003-4669-9091 Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365, Rio de Janeiro CEP 21040 - 900, Brazil. & Programa de Pós-graduação em Biodiversidade e Saúde (PPGBS), Instituto Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365, Rio de Janeiro CEP 21040 - 900, Brazil & sferreiraantoniocarlos @ gmail. com; https: // orcid. org / 0000 - 0003 - 4669 - 9091 sferreiraantoniocarlos@gmail.com Author Vieira, Fabiano Matos Universidade Federal do Vale do São Francisco (Univasf). Rodovia BR- 407, KM 12 Lote 543 S / n Projeto de Irrigação Nilo Coelho, Petrolina, 56300 - 000, Brazil. Author Silva, Diego César Nunes Da Universidade Federal do Vale do São Francisco (Univasf). Rodovia BR- 407, KM 12 Lote 543 S / n Projeto de Irrigação Nilo Coelho, Petrolina, 56300 - 000, Brazil. & diego. nunes @ univasf. edu. br Author Ribeiro, Leonardo Barros 0000-0003-4491-0236 Universidade Federal do Vale do São Francisco (Univasf). Rodovia BR- 407, KM 12 Lote 543 S / n Projeto de Irrigação Nilo Coelho, Petrolina, 56300 - 000, Brazil. & leonardo. ribeiro @ univasf. edu. br; https: // orcid. org / 0000 - 0003 - 4491 - 0236 leonardo.ribeiro@univasf.edu.br Author Ferreira, Jayelen Alves 0000-0001-8372-0510 Universidade Federal do Vale do São Francisco (Univasf). Rodovia BR- 407, KM 12 Lote 543 S / n Projeto de Irrigação Nilo Coelho, Petrolina, 56300 - 000, Brazil. & Programa de Pós-graduação em Ciências Veterinária no Semiárido, Univasf. Rodovia BR- 407, KM 12 Lote 543 S / n Projeto de Irrigação Nilo Coelho, Petrolina, 56300 - 000, Brazil. & JayelenAlves @ live. com; https: // orcid. org / 0000 - 0001 - 8372 - 0510 lves@live.com Author Muniz-Pereira, Luís Cláudio 0000-0002-7468-6274 Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365, Rio de Janeiro CEP 21040 - 900, Brazil. & Programa de Pós-graduação em Biodiversidade e Saúde (PPGBS), Instituto Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365, Rio de Janeiro CEP 21040 - 900, Brazil & lmuniz @ ioc. iocruz. br; https: // orcid. org / 0000 - 0002 - 7468 - 6274 lmuniz@ioc.iocruz.br text Zootaxa 2021 2021-05-31 4980 1 185 200 journal article 6104 10.11646/zootaxa.4980.1.12 8961efc4-38a4-45ca-ae96-7dc85da95579 1175-5326 4882889 BCC6F4E1-C924-466F-8328-FFFAC42A9D6E Parapharyngodon hispidus n. sp. ( Figs. 1 and 2 ) General: Small, robust, whitish nematodes. Cuticle with prominent annulations beginning just behind anterior extremity and continuing to anus or cloacal aperture. Sexual dimorphism evident, males with approximately 30% of total body length of females. Males with triangular mouth aperture, with internal cuticular projections, cephalic papillae not visible, two lateral amphids, near lateroventral side of mouth ( Figs. 1C , 2B ). Females with star shaped mouth aperture; surrounded by three bilobed lips, one dorsal and two lateroventral, two amphids each opening on lateral lips ( Figs. 1D , 2C ). Oxyuriform oesophagus, ending in valved oesophageal bulb ( Figs. 1A, B ). Nerve ring at level of first third of oesophagus ( Figs. 1A, B ). Excretory pore far posterior to oesophageal bulb in both males and females ( Figs. 1A, B ). Males without caudal alae; caudal appendage directed dorsally ( Figs. 1E, F , 2D ). Lateral alae only in males ( Figs. 1A , 2A ). Male (Based on 10 adult mature specimens, measurements of holotype in parentheses) : Total body length 3.2–3.6 (3.2) mm, body width at level of oesophagus-intestinal junction 225–375 (270). Total oesophagus length 525–710 (525); corpus 420–530 (420) long, oesophageal bulb 110–140 (115) long, and 120–150 (125) wide. Nerve ring 138–163 (138) and excretory pore 1.2–1.5 (1.5) mm from anterior end. Lateral alae present ( Figs. 1A , 2A ) 1.7– 2.1 (1.7) mm long, beginning at the level of the oesophageal bulb and ending far distant to cloacal aperture. Cloacal lips smooth, not echinate ( Figs. 1F , 2D–F ). Posterior region with four pairs of caudal papillae ( Figs. 1E, F , 2D ); the first pair is subventral located immediately anterior to cloacal aperture; the second is lateral, located posterior to cloacal aperture; third pair is subventral, at level of the second pair and immediately posterior to cloacal aperture; and the fourth pair is located on caudal appendage Figs. 1E, F , 2D–F ). One spicule well sclerotized 110–123 (110) long, terminating in a sharp tip ( Figs. 1E, F ). Gubernaculum absent. Tail conical 135–305 (175) (including caudal appendage), with a subdorsal caudal appendage 57–95 (75) long ( Figs. 1E, F , 2E ) . Female (Based on 10 adult mature specimens, measurements of allotype in parentheses): Total body length 7.4–10.5 (10) mm, body width at level of oesophagus-intestinal junction 720–1,160 (900). Total oesophagus length 1.3–1.7 (1.6) mm; corpus 1–1.4 (1.3) mm, oesophageal bulb 220–250 (240) long, and 250–310 (310) wide. Nerve ring 192–250 (230) and excretory pore 2.2–3.3 (2.8) mm from anterior end. Vulva not prominent ( Fig. 1H ), equatorial, 3.6–5.5 (5) mm from anterior end, followed by short vagina and ovijector direct posteriorly. Didelphic, uteri amphidelphic, and ovaries directed anteriorly. Both ovaries encircling isthmus and anterior region of oesophageal bulb ( Fig. 1B ). Eggs subovate, 67–100 long, 37–60 wide, flattened on one side, with one subapical operculum, without polar filament, early stages of cleavage in the ovijector ( Figs. 1H, J, K ). Eggshell thick, with punctated surface. Tail 400–590 (590) long (including spike tip) ( Figs. 1G , 2G ), corresponding approximately to 5.5% of total body size (mean proportional size, based on the proportional tail sizes of all females analyzed), with short spiked tip, 190–245 (210) long. Taxonomic summary Type host : Tropidurus hispidus (Spix) ( Squamata : Tropiduridae ) (Neotropical Lava Lizard, calango-de-muro) Type locality : Campus de Ciências Agrárias (Agrarian Sciences Campus) (CCA) ( 09°19’41”S , 40°32’59”W ) of the Universidade Federal do Vale do São Francisco (Univasf), municipality of Petrolina, state of Pernambuco , Brazil . Site of infection : large intestine. Prevalence : 56.85% (112 infected hosts) Mean intensity : 4.13 ± 11.96 parasites per infected hosts Mean abundance : 2.35 ± 10.56 parasites per analyzed hosts Range of infections: 1–21 Type material : Holotype male (CHIOC 38994a)), allotype female (CHIOC 38994b), 2 males and 4 females paratypes (CHIOC 38994c). FIGURE 1. Parapharyngodon hispidus n. sp. A—anterior region of body, male, ventral view; B—anterior region of body, female, lateral view; C—anterior end, male, apical view; D—anterior end, female, apical view; E—posterior region, male, lateral view; F—posterior region, male, ventral view; G—posterior region, female, lateral view; H—vulva and ovijector, lateral view; I—egg near to ovary end (isolated); J—egg in ovijector, lateral view (isolated), K—egg in ovijector, ventral view (isolated). Etymology: The species name of the hosts species is used as a noun in apposition to Parapharyngodon .. Remarks: The main feature considered for the differentiation of species in Parapharyngodon and Thelandros Wedl species ( Oxyurida : Pharyngodonidae ) is the egg morphology and development ( Bursey et al . 2013 , Velarde-Aguilar et al . 2015, Rizvi et al . 2017 ). Therefore, the specimens evaluated in the present study were classified as Parapharyngodon since they present eggs with a subterminal operculum and in the early stages of cleavage in ovijector. With the description of the new species the genus Parapharyngodon currently includes 55 valid species ( Bursey & Goldberg 2015 , Velarde-Aguilar et al . 2015 , Araujo Filho et al . 2015 , Garduño-Montes de Oca et al . 2016 , Ramallo et al . 2016 , Rizvi et al . 2017 , Pereira et al . 2017 , Santos et al . 2018 ), which can be differentiated by zoogeographic region, the presence or absence of body alae in males and females; male characteristics, such as the number and arrangement of caudal papillae, the morphology of anterior border of cloacal aperture, and the size and type of distal end of spicules; and female characteristics, such as position of the ovaries relative to the oesophageal bulb, the morphology of eggshell, and tail ( Bursey et al . 2013 , 2015 , Velarde-Aguilar et al . 2015 , Rizvi et al . 2017 , Pereira, 2017 ). In the Neotropical realm, ten valid species of Parapharyngodon have been described so far ( Table 1 ). Parapharyngodon hispidus n. sp. has four pairs of caudal papillae, as do four other Neotropical species, namely, P. bainae Pereira, Sousa & Souza Lima , P. silvoi , P. sanjuanensis Ramallo, Bursey, Castillo & Acosta , and P. sceleratus . Parapharyngodon hispidus n. sp. , P. silvoi , and P. sceleratus have a smooth anterior border of cloacal aperture, differing from the echinate anterior border of the cloaca of P. bainae and P. sanjuanensis ( Pereira et al . 2011 , 2018 , Ramallo et al . 2016 ). Parapharyngodon hispidus n. sp. differs from P. silvoi , and P. sceleratus as the latter two have an unpaired post cloacal papilla ( Freitas 1957 , Vicente et al . 1993 , Araujo Filho et al . 2015 , Velarde-Aguilar et al . 2015 ), which is absent in P. hispidus n. sp. FIGURE 2. Parapharyngodon hispidus n. sp. A—anterior region of body, male, ventral view; B—anterior end, male, apical view (dorsal side is at the top of the image); C—anterior end, female, apical view (dorsal side is at the bottom of the image); D—caudal region, male, latero-ventral view; E—cloacal region, male, latero-ventral view; F—cloacal region, male, ventral view., G—posterior region, female, ventral view. Abbreviation use: *, post cloacal medial pair of papillae; cl, cloacal lip; la, lateral alae. TABLE 1. Characters of species of Parapharyngodon Chatterji from the Neotropical realm, used for differentiation.

Species	Type host	Locality (Country)	Males
Spicule (µm)	Spicule tip	Caudal Papillae distribution (pre:ad:post cloacal)	Unpaired post cloacal papilla	Clocal lip
P. alvarengai Freitas	Trachylepis maculata (Gray) (= Mabuya maculata ) ( Squamata : Scincidae )	Fernando de Noronha, state of Pernambuco (Brazil)	80–100	sharp	1:1:1	No	Smooth
P. bainae Pereira, Sousa & Souza Lima	Tropidurus torquatus (Wied-Neuwied) ( Squamata : Tropiduridae )	Toledos, state of Minas Gerais (Brazil)	100–140	sharp	1:0:3	No	Echinate
P. riojensis Ramallo, Bursey & Goldberg	Phymaturus punae Cei, Etheridge, and Videla ( Squamata : Liolaemidae )	Province of La Rioja, (Argentina)	90–110	sharp	1:0:2	Yes	Echinate
P. silvoi Araujo Filho, Brito , Al- meida, Morais & Avila	Dermatonotus muelleri (Boettger) ( Anura : Microhylidae )	Exu, state of Pernam- buco (Brazil)	57–71	blunt	1:1:2	Yes	Smooth
P. sanjuanensis Ramallo, Bursey, Castillo & Acosta	Phymaturus williamsi Lobo, Laspiur & Acosta ( Squamata : Liolaemidae )	Province of San Juan (Argentina)	80–180	sharp	2:0:2	No	Echinate
P. hugoi Pereira, Campião, Luque & Tavares	Trachycephalus typhonius (Linnaeus) ( Anura : Hylidae )	Miranda, State of Mato Grosso do Sul (Brazil)	40–58	sharp	0:2:1	No	Echinate
P. largitor Alho & Rodrigues	Hemidactylus mabouia (Moreau de Jon- nès) ( Squamata : Gekkonidae )	State of Rio de Janeiro (Brazil)	54–68	sharp	0:2:1	Yes	Smooth
P. sceleratus (Travassos)	T. torquatus	Rio de Janeiro, State of Rio de Janeiro (Brazil)	82–100	Sharp	2:1:1	Yes	Smooth
P. verrucosus Freitas & Dobbin Jr	Diploglossus lessonae Peracca ( Squamata : Diploglossidae )	João Alfredo, State of Pernambuco (Brazil)	54–68	Sharp	1:1:1	Yes	Smooth
P. politoedi Santos, Argolo, Santos, Rodrigues, Gonzaléz, Santos & Melo	Osteocephalus taurinus Steindachner ( Anura : Hylidae )	Caxiuanã National Forest, State of Pará (Brazil)	53–75	sharp	1:1:1	No	Echinate
P. hispidus n. sp.	Tropidurus hispidus (Spix) ( Squamata : Tropiduridae )	Petrolina, State of Per- nambuco (Brazil)	110–123	sharp	1:0:3	No	Smooth

......continued on the next page TABLE 1. (Continued)

Species	Females	Reference
Ovary location	Vulva	Tail terminus	Eggs hell
P. alvarengai Freitas	Pre-bulbar	Equatorial	Spike stout	Thin, smooth	Freitas (1957)
P. bainae Pereira, Sousa & Souza Lima	Pre-bulbar	Equatorial	Spike stout	Thick, punctated	Pereira et al . (2011 , 2018 )
P. riojensis Ramallo, Bursey & Goldberg	Post bulbar	Post equatorial	Spike stout	Thin, punctated	Ramallo et al . (2002)
P. silvoi Araujo Filho, Brito, Almeida, Morais & Avila	Post bulbar	equatorial	Spike stout	Thick, punctated	Araujo Filho et al . (2015)
P. sanjuanensis Ramallo, Bursey, Castillo & Acosta	Post bulbar	equatorial	Spike stout	Thin, punctated	Ramallo et al . (2016)
P. hugoi Pereira, Campião, Luque & Tavares	Post bulbar	Pre equatorial	Conical	Thin	Pereira et al . (2017)
P. largitor Alho & Rodrigues	Pre bulbar	Pre equatorial	Spike stout	Thin, smooth	Alho & Rodrigues (1963)
P. sceleratus (Travassos)	Pre bulbar	Equatorial	Spike stout	-	Travassos (1923) , Freitas (1957) , Vicente et al . (1993) , Velarde-Aguilar et al . (2015)
P. verrucosus Freitas & Dobbin Jr	Pre bulbar	Equatorial	Spike stout	-	Freitas & Dobbin Jr (1959)
P. politoedi Santos, Argolo, Santos, Rodrigues, Gonzaléz, Santos & Melo	Post bulbar	Pre equatorial	Conical	Thick	Santos et al . (2018)
P. hispidus n. sp.	Pre bulbar	equatorial	Spike stout	Thick, punctated	Current study

TABLE 2. Characters of species of Parapharyngodon Chatterji having 4 pairs of caudal papillae, unpaired post cloacal papilla absent, and smooth cloacal lips, used for differentiation.

Species	Type host	Country	Males	Females	References
(Biogeographical realm)	Spicule (µm)	Spicule tip	Tail tip	Egg
P. baueri Bursey & Goldberg	Acontias kgalagadi (Lamb, Biswas & Bauer) ( = Typhlosaurus lineatus ) ( Squamata , Scincidae )	Botswana (Afrotropical)	79–98	Sharp	Stout spike	Analate, shell smooth	Bursey & Goldberg (2007)
P. californiensis Read & Amrein	Xantusia vigilis Baird ( Squamata , Xantusiidae )	USA (Nearctic)	53–76	Sharp	Stout spike	Analate, shell smooth	Read & Amrein (1952)
P. jairaipurii Rizvi & Bursey	Hemidactylus flaviviridis Ruppell ( Squamata , Gekkonidae )	India (Oriental)	60–75	Sharp	Stout spike	Analate, shell punctate	Rizvi & Bursey (2013)
P. skrjabini Vakker	Pseudopus apodus (Pallas) ( Squamata , Anguidae ) (= Ophisaurus apodus )	Kazakhstan (Palearctic)	139–176	Sharp	Thin spike	Analate, shell smooth	Rizvi & Bursey (2013) Bursey & Goldberg (2015) Rizvi et al . (2017)
P. striatus Singh & Malhotra	H. flaviviridis	India (Oriental)	79–92	Blunt	Stout spike	Not described	Gupta et al . (2009) Bursey & Goldberg (2015) Rizvi et al . (2017)
P. hispidus n. sp.	Tropidurus hispidus (Spix) ( Squamata , Tropiduridae )	Brazil (Neotropical)	110–123	Sharp	Stout spike	Analate, shell punctate	Current study

We highlight some considerations about two Neotropical Parapharyngodon species. Rizvi & Bursey (2013) , Bursey & Goldberg (2015) , and Rizvi et al . (2017) considered the females of P. alvarengai as featuring a conical tail with no spike. However, the original description of this species (see Freitas 1957 ) clearly shows a stout spike, which was also observed by Velarde-Aguilar et al . (2015) and Pereira et al . (2017) . In the description of P. silvoi, Araujo Filho et al . (2015) describe females having ovaries extending beyond the oesophageal bulb (ovaries pre bulbar). However, we analyzed the species’ drawings in the original description and observed that the drawn female had post bulbar ovaries. Thus, we consider here the characteristics of P. silvoi demonstrated in the graphic representations. Among the species of other zoogeographic distribution, P. hispidus n. sp. belongs to a group with four pairs of caudal papillae, without unpaired post cloacal papilla, and smooth cloacal lips ( Table 2 ). The species composing this group are Parapharyngodon baueri Bursey & Goldberg (Afrotropical realm), P. californiensis Read & Amrein (Nearctic realm), P. jairaipurii Rizvi & Bursey (Oriental realm), P. skrjabini Vakker (Palearctic realm), and P. striatus Singh & Malhotra (Oriental realm) ( Table 2 ). Parapharyngodon jairaipurii , described for Hemidactylus flaviviridis Ruppell ( Squamata , Gekkonidae ) from India , is the only species presenting the same set of characteristics of spicule tip (sharp pointed), female tail end (stout spike), and eggshell morphology (punctate) ( Rizvi & Bursey 2013 ) ( Table 2 ). Although P. hispidus n. sp. and P. jairaipuri share key characteristics used to diagnose species, including sharppointed spicules, female tail ending with a stout spike, and eggs with punctated shells, other morphological and morphometric characteristics differentiate these species ( Table 3 ). The main characteristics differentiating these species are the size of spicules (spicules of P. jairaipuri are around 55% of the size spicules of P. hispidus n. sp. ) and the arrangement of the caudal papillae (two pairs of adcloacal papillae in P. jaraipuri which are absent in P. hispidus n. sp. ) ( Rizvi & Bursey 2013 ) ( Table 3 ).