New records of helminths of Sceloporus pyrocephalus Cope (Squamata, Phrynosomatidae) from Guerrero and Michoacán, Mexico, with the description of a new species of Thubunaea Seurat, 1914 (Nematoda, Physalopteridae)

Edgar Uriel Garduño-Montes de Oca; Jorge D. López-Caballero; Rosario Mata-López

doi:10.3897/zookeys.716.13724

Abstract

A total of 61 specimens of the Red-headed Spiny Lizard Sceloporus pyrocephalus Cope (Phrynosomatidae) collected during the breeding season (June/July 2003, 2004 and 2005) from Western Mexico were examined for helminths. The morphological characterization of the helminths found was made through light microscopy and scanning electron microscopy. Nine taxa of helminths were identified, two cestodes: Mesocestoides sp. and Oochoristica sp., and seven nematodes: Parapharyngodon ayotzinapaensis Garduño-Montes de Oca, Mata-López & León-Règagnon, 2016, Parapharyngodon tikuinii Garduño-Montes de Oca, Mata-López & León-Règagnon, 2016, Parapharyngodon sp., Physalopterinae gen. sp., Skrjabinoptera scelopori Caballero-Rodríguez, 1971, Strongyluris similis Caballero, 1938 and a new species of Thubunaea Seurat, 1914. Larvae of Mesocestoides sp. and Physalopterinae gen. sp. were found in the body cavity and digestive tract, respectively. Excluding the species of Parapharyngodon Chatterji, 1933, S. pyrocephalus is recorded for the first time as a host of the remaining seven taxa of helminths. Additionally, Thubunaealeonregagnonae sp. n. is described and illustrated as a new nematode species, parasite of S. pyrocephalus from Mexico. This new species can be differentiated from the majority of its congeners by the absence of spicules, the particular pattern of caudal papillae in males and the small ratio of oesophagus length:male total body length (0.1–0.16).

Keywords

Anoplocephalidae , Helminths, Heterakidae , Mesocestoididae , Pharyngodonidae , Physalopteridae , Reptilia , Thubunaea , Western Mexico.

Introduction

Mexico is ranked as a country with the second highest diversity of reptiles, 864 species of which 493 are endemic to the country (Flores-Villela and García-Vázquez 2014). Lizards are the species-richest reptilian group with 417 species, and among them the Phrynosomatidae are the most diverse family (representing 15.9% of the total lizard diversity from Mexico). Despite this, our knowledge regarding the helminth fauna of this family is limited. Parasite records exist for only 15.3% of the total taxa within the Phrynosomatidae (Paredes-León et al. 2008).

Sceloporus Wiegmann (Phrynosomatidae) is a genus of New World lizards composed of 92 nominal species, of which 59 are endemic to Mexico (Uetz et al. 2016). Particularly, Sceloporus pyrocephalus Cope is an endemic lizard of Western Mexico associated with streams and rivers within tropical deciduous and semi-deciduous forest (Uetz et al. 2016), and distributed along the Pacific coast of the southwestern states of Jalisco, Colima, Michoacán and Guerrero as well as Central Mexico, and Southern Morelos. Despite some efforts to characterize the parasites of this species of lizard (Calisi et al. 2008), current knowledge of its helminth fauna is still far from being complete.

The purpose of the present study is to report on the helminth fauna of S. pyrocephalus, including the description of a new species of Thubunaea Seurat, 1914.

Materials and methods

A total of 61 specimens of S. pyrocephalus were collected during the breeding season from June/July in 2003, 2004 and 2005 (permit FAUT-0056 issued to Virginia León-Règagnon by Secretaría del Medio Ambiente y Recursos Naturales, SEMARNAT). The specimens were captured by noosing or by hand in 12 localities from Michoacán state, and three localities from Guerrero state, Mexico (Table 1). These localities include tropical-wet and hot-semi-arid climates and elevations ranging from 18–1462 m a.s.l. Lizards were euthanized with an intraperitoneal overdose of pentobarbital sodium. The mouth, peritoneal cavity, and all internal organs were examined for helminths under a stereoscopic microscope. Helminths obtained were counted, fixed, and preserved following the procedure proposed by Lamothe-Argumedo (1997). Nematodes and cestodes were fixed in hot 4% and 10% formaldehyde solution, respectively, and stored in 70% ethanol. For morphological examination, nematodes were cleared in alcohol-glycerol, and mounted on temporary slides. Cestodes were stained with Mayer’s paracarmine and mounted on permanent slides using Canada balsam. Preserved specimens were observed under a light microscope. Original drawings were made with an Olympus BX53 microscope equipped with a drawing tube. For scanning electron microscopy (SEM), worms were dehydrated through a graded series of ethanol and then critical point dried with carbon dioxide, coated with a gold/palladium mixture using a Q150R Modular Coating System, and examined in a Hitachi S-2460N microscope and SU1015 SEM (Hitachi). Measurements of the new species are presented in micrometres, unless otherwise indicated; the range is followed by the mean in parentheses. Quantitative descriptors of parasite populations were calculated based on Bush et al. (1997). The helminths were deposited in the Colección Nacional de Helmintos (CNHE), Instituto de Biología (UNAM). Specimens of lizards were deposited in the Colección Herpetológica, Museo de Zoología, Facultad de Ciencias, UNAM (MZFC-HE) and the Collection of the Amphibian and Reptile Diversity Research Center at the University of Texas at Arlington (ARDRC-UTA).

Table 1.

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Sampling localities in Mexico for Sceloporus pyrocephalus examined in this study.

Locality	GPS coordinates	Collection	Accession number
Michoacán
Maruata	18°16'29"N, 103°20'51"W	July 2004	58252 ^‡, JAC-25491, JAC-25513
Caleta de Campos	18°04'48"N, 102°45'56"W	July 2004	58245^‡, 58246^‡, JAC-25529
Aquila	18°35'27.96"N, 103°34'0.12"W	July 2003	17445^†-17447^†
Nuevo Corongoros	19°06'14.5"N, 102°53'52"W	July 2005	18321^†, 18322^†, 18324^†
Arteaga	18°38'48.48"N, 101°58'6.24"W	July 2005	18349^†, JAC-26111, JAC-26112, JAC-26114, JAC-26115
La Huacana	18°40'24.2"N, 101°59'42.5"W	July 2005	18320^†, 18343^†-18348^†
Los Laureles	18°58'14"N, 103°05'27"W	June 2004	58221^‡, JAC-24752
San Isidro Tecuiluca	19°04'33"N, 102°53'37"W	June 2004	58232^‡, 58235^‡, JAC-24776, JAC-24778
Los Avillos	19°02'19"N, 102°58'28"W	June 2004	JAC-24755
Buenavista Tomatlán	19°10'35.8"N, 102°39'48.6"W	July 2005	18313^†-18315^†, 18317^†, 18318^†, 18332^†, 18334^†-18337^†, 18340^†, JAC-26102
Apatzingan	19°07'29"N, 102°24'05"W	July 2003	53473^‡, 53474^‡
Lombardia	19°10'35"N, 102°03'48"W	June 2004	58207^‡, 58213^‡, 58216^‡, 58238^‡, 58240^‡, JAC-24718, JAC-24878
Guerrero
Coyuquilla	17°17'48.12"N, 101°02'48.12"W	July 2004	JAC-25311
Tecpan de Galeana	17°10'37.20"N, 100°35'43.1"W	July 2005	JAC-25575, JAC-26136-JAC-26141
Coyuca de Catalán	17°59'41.2"N, 101°11'43.5"W	July 2004	JAC-25218

Results

A total of nine helminth taxa was found parasitizing S. pyrocephalus: two cestodes and seven nematodes (Table 2). Only Mesocestoides sp. and Physalopterinae gen. sp. were found as larval stages in the body cavity and digestive tract, respectively. The remaining taxa were found as adults located in the intestine. In the following section, we list the helminth species from S. pyrocephalus found during the present study, along with previous records of each parasite taxon in different Sceloporus spp. from Mexico, where applicable.

Table 2.

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Helminth taxa collected from Sceloporus pyrocephalus Cope (Phrynosomatidae) at various localities in Mexico. Values presented for 3 locality are number of hosts examined (n), followed by prevalence (P%) and mean abundance (MA – range or number of specimens recovered when number of hosts parasitized was 1).

Locality		Cestoda		Nematoda
Locality		Mesocestoides sp.^{†, L}	Oochoristica sp.^{‡, A}	Parapharyngodon ayotzinapaensis Garduño-Montes de Oca et al., 2016 ^{§, A}	Parapharyngodon tikuinii Garduño-Montes de Oca et al., 2016 ^{§, A}	Parapharyngodon sp.^{§, A}	Physalopterinae gen. sp.^{\|, L}	Skrjabinoptera scelopori Caballero-Rodríguez, 1971^{‡, A}	Strongyluris similis Caballero, 1938^{§, A}	Thubunaea leonregagnonae sp. n.^{\|, A}
Michoacán
Maruata	n							3	n=3
	P%							100	33.33
	MA							13.33 (7–24)	2.33 (7)
Caleta de Campos	n							3	3	3
	P%							33.33	33.33	100
	MA							7.67 (23)	2.67 (8)	17.67 (9–23)
Aquila	n	3		3		3
	P%	33.33		33.33		66.67
	MA	42.33 (127)		5.66 (17)		1.33 (4)
Nuevo Corongoros	n								3
	P%								100
	MA								6 (2–11)
Arteaga	n			7	7	7				7
	P%			14.29	28.57	14.29				57.14
	MA			0.28 (2)	0.71 (2–3)	0.28 (2)				4.28 (3–18)
La Huacana	n				7			7		7
	P%				14.29			28.57		85.71
	MA				0.14 (1)			2 (1–13)		9.57 (1–17)
Los Laureles	n								4
	P%								50
	MA								4.75 (5–14)
San Isidro Tecuiluca	n				5	5
	P%				20	60
	MA				0.2 (1)	0.6 (3)
Los Avillos	n				1
	P%				100
	MA				– (1)
Buenavista Tomatlán July 2005	n	22			22	22	22
	P%	4.54			9.09	27.27	18.18
	MA	0.13 (3)			0.23 (2–3)	1.14 (1–8)	11.32 (14–235)
Apatzingan	n				2	2
	P%				50	50
	MA				0.5 (1)	0.5 (1)
Lombardia	n		12	12	12	12	12
	P%		8.3	16.67	16.67	16.67	8.33
	MA		0.08 (1)	0.66 (2–4)	0.33 (1–3)	0.33 (4)	2.42 (29)
Guerrero
Coyuquilla	n			2	2
	P%			50	50
	MA			1.5 (3)	0.5 (1)
Tecpan de Galeana	n			7		7				7
	P%			14.29		57.14				14.29
	MA			1.71 (12)		2.14 (3–4)				1 (7)
Coyuca de Catalán	n					1
	P%					100
	MA					– (4)

Hosts parasitized/ hosts examined		2/61	1/61	6/61	11/61	20/61	5/61	6/61	7/61	14/61
Specimens recovered		130	1	42	19	58	278	77	52	157
Intensity range		3–27	–	2–17	1–5	1–25	29–249	14–40	7–19	7–67

Phylum Platyhelminthes Gegenbaur, 1859

Class Cestoda Rudolphi, 1808

Family Mesocestoididae Fuhrmann, 1907

Genus Mesocestoides Vaillant, 1863

Mesocestoides sp.

Specimens deposited

CNHE 9464, 9465.

Other hosts

Sceloporus jarrovi Cope in Chihuahua, Morelos and San Luis Potosí (Goldberg et al. 1996); S. grammicus Wiegmann in Mexico City (Goldberg et al. 2003); S. torquatus Wiegmann in Querétaro (Goldberg et al. 2003).

Remarks

Four species of Mesocestoides are distributed in Mexico in carnivorous mammals: M. bassarisci MacCallum, 1921 in Bassariscus astutus Lichtenstein (Procyonidae) and M. lineatus (Goeze, 1782) in Mephitis macroura Lichtenstein (Mephitidae), both from Guerrero; M. variabilis Mueller, 1928 and M. vogae Etges, 1991 in Canis lupus familiaris Linnaeus (Canidae) from Mexico City (Paredes-León et al. 2008). Unfortunately, the specimens found in S. pyrocephalus could not be identified to species level because they were at the tetratiridium larval stage. Molecular analyses are needed to determinate the species identity of the larvae found in reptilian hosts, which serve as intermediate hosts (Santoro et al. 2012).

Family Anoplocephalidae Cholodkovsky, 1902

Genus Oochoristica Lühe, 1898

Oochoristica sp.

Specimens deposited

CNHE 9469.

Remarks

Eight species of Oochoristica have been recorded in Mexico: O. acapulcoensis Brooks, Pérez-Ponce de León & García-Prieto, 1999; O. leonregagnonae Arizmendi-Espinosa, García-Prieto & Guillén-Hernández, 2005; O. osheroffi Meggitt, 1934 and O. whitentoni Stellman, 1939, all parasites of Ctenosaura pectinata Weigmann (Iguanidae) from Acapulco, Guerrero (Brooks et al. 1999), Mixtequilla, Oaxaca (Arizmendi-Espinoza et al. 2005), Alpuyeca, Morelos (Flores-Barroeta et al. 1960), and Iguala, Guerrero (Flores-Barroeta 1955). Oochoristica whitfieldi Guillén-Hernández, García-Prieto & Arizmendi-Espinosa, 2007 was found parasitizing C. oaxacana Köhler & Hasbun (Iguanidae) (Guillén-Hernández et al. 2007); O. parvula Stunkard, 1938 was found in Coleonyx elegans Gray (Eublepharidae) from Oxkutzcab, Yucatán (Stunkard 1938); O. phrynosomatis Harwood, 1932 in Phrynosoma braconnieri Dugès, and P. taurus Duméril & Bocourt (Phrynosomatidae) from Cacaloapan and Caltepec, both in Puebla (Goldberg and Bursey 1991). Oochoristica scelopori Voge & Fox, 1950 was found infecting species of the family Phrynosomatidae: S. jarrovi (Goldberg et al. 1996); S. parvus Smith, S. grammicus, S. megalepidurus Smith, S. variabilis Wiegmann, S. mucronatus Cope, and P. ditmarsi Stejneger (Goldberg et al. 2003). Only one adult specimen of Oochoristica was found in the present study; however, it was not identified to specific level due to the absence of gravid proglottids.

Phylum Nematoda Cobb, 1932

Class Chromadorea Inglis, 1983

Family Pharyngodonidae Travassos, 1920

Genus Parapharyngodon Chatterji, 1933

Parapharyngodon ayotzinapaensis Garduño-Montes de Oca, Mata-López & León-Règagnon, 2016

Specimens deposited

CNHE 9432–9438.

Remarks

Eleven species of Parapharyngodon have been recorded in Mexico (Garduño-Montes de Oca et al. 2016), eight of them endemic, representing 10% of the world diversity of this genus. The high species richness of Parapharyngodon is probably related to the geographical and environmental heterogeneity of this region, and was recently revealed by parasitological surveys of host species not considered in previous studies (Jiménez et al. 2008, Bursey and Goldberg 2015, Velarde-Aguilar et al. 2015, Garduño-Montes de Oca et al. 2016).

Parapharyngodon tikuinii Garduño-Montes de Oca, Mata-López & León-Règagnon, 2016

Specimens deposited

CNHE 9439–9447.

Remarks

See P. ayotzinapaensis remarks.

Parapharyngodon sp.

Specimens deposited

CNHE 9448–9454, 9470, 9471.

Remarks

Female specimens of Parapharyngodon sp. were recovered from hosts in the same localities as P. ayotzinapaensis and P. tikuinii. The almost identical morphology of females in both species did not allow us to discriminate between them on species level (Garduño-Montes de Oca et al. 2016).

Family Heterakidae Railliet & Henry, 1912

Genus Strongyluris Müller, 1894

Strongyluris similis Caballero, 1938

Specimens deposited

CNHE 9455–9459.

Other hosts

S. torquatus in Mexico City (Cid del Prado 1971); S. jarrovi in Durango, Guanajuato, Hidalgo, Morelos, San Luis Potosí, Sinaloa, Sonora, Tamaulipas and Veracruz (Goldberg et al. 1996); S. grammicus and S. mucronatus in localities not further specified (Goldberg et al. 2003); S. formosus Wiegmann in Oaxaca (Goldberg et al. 2003).

Remarks

Specimens recovered during the present study share certain morphological characters with S. panamaensis Bursey, Goldberg & Telford, 2003 and S. similis such as spicule length and number of caudal papillae. Our specimens were identified as S. similis since they possess two pairs of lateral subterminal papillae at the base of the caudal appendage (Caballero 1938), which is a diagnostic feature of this species, contrary to the three pairs of papillae observed at the base of the caudal appendage in S. panamaensis (Bursey et al. 2003).

Family Physalopteridae (Railliet, 1893) Leiper, 1908

Subfamily Physalopterinae Railliet, 1893

Physalopterinae gen. sp.

Specimens deposited

CNHE 9466–9468.

Other hosts

Abbreviata terrapenis Hill, 1941 in S. jarrovi from Tamaulipas (Goldberg et al. 1996). Physaloptera retusa Rudolphi, 1819 in S. jarrovi from Aguascalientes, Chihuahua, Coahuila, Durango, Guanajuato, Morelos, Nuevo León, Querétaro, San Luis Potosí, Sinaloa, Sonora and Tamaulipas (Goldberg et al. 1996); in S. acanthinus Bocourt from Motozintla, Chiapas (Caballero 1951); in S. jarrovi (Goldberg et al. 1996) and S. parvus (Goldberg et al. 2003) from Hidalgo; in S. formosus from Oaxaca (Goldberg et al. 2003); in S. mucronatus from Puebla (Goldberg et al. 2003); in S. torquatus from Zacatecas (Goldberg et al. 2003). Skrjabinoptera phrynosoma (Ortlepp, 1922) Schulz, 1927 in S. jarrovi from Guanajuato (Goldberg et al. 1996); in S. spinosus Wiegmann from Actopan, Hidalgo (Caballero 1937); in S. jarrovi from Querétaro (Goldberg et al. 1996), and finally, in S. grammicus and S. variabilis from localities not further specified (Goldberg et al. 2003).

Remarks

Representatives of the subfamily Physalopterinae use ants and beetles as intermediate hosts, which are part of the diet of S. pyrocephalus. By eating that sort of prey, this group of lizards becomes a potential intermediate or paratenic host of these nematodes (Petri 1950, Schell 1952, Lee 1957, Kabilov 1980).

Genus Skrjabinoptera Schulz, 1927

Skrjabinoptera scelopori Caballero-Rodríguez, 1971

Specimens deposited

CNHE 9460–9463.

Other hosts

S. grammicus in San Andrés Totoltepec and San Ángel, Mexico City (CNHE); S. torquatus in Mexico City (Caballero-Rodríguez 1971). Skrjabinoptera sp. in S. torquatus from San Ángel, Mexico City (Cid del Prado 1971).

Remarks

Skrjabinoptera is a genus of nematodes poorly represented around the world with only 10 species described as parasites, mainly of lizards, and only one species recorded from a snake (Rudolphi 1819). In Mexico, only S. scelopori has been recorded in three species of lizards: S. torquatus, S. grammicus, and Phyllodactylus lanei Smith (Gekkonidae) (Goldberg and Bursey 2000, Paredes-León et al. 2008). Sceloporus pyrocephalus is the fourth host species recorded for this helminth in the country.

Subfamily Thubunaeinae Sobolev, 1949

Genus Thubunaea Seurat, 1914

Thubunaea leonregagnonae sp. n.

http://zoobank.org/E2747F2B-1083-45B4-876C-D83E13A9F3AA

Figs 1A–H; 2A–F

Type host

Sceloporus pyrocephalus Cope (Squamata: Phrynosomatidae).

Symbiotype

MZFC-HE 18345

Type locality

Los Pocitos, La Huacana, Michoacán, Mexico (18°40'24.2"N, 101°59'42.5"W). Collected on July 7, 2005.

Site in host

Stomach.

Prevalence and intensity of infection

23% (14 of 61 hosts examined), with a mean intensity of 11 (7–67).

Type specimens

Holotype: CNHE 9426 (1 male); allotype: CNHE 9427 (1 female); paratypes CNHE 9428, 9429, 9430 and 9431 (9 females and 7 males).

Etymology

This species is named in honour of Virginia León-Règagnon (Instituto de Biología, UNAM), who was the mentor of the authors of this paper, and for her valuable contribution to our knowledge of helminth parasites in Mexico.

General description

Medium-sized nematodes, filiform body, cuticle with fine transverse striations along entire body. Males smaller than females. Round cephalic plate in both sexes (Figs 1B, 2B). Deirids symmetrical, simple with rounded tip (Fig. 2A, C), located immediately posterior to nerve ring. Mouth with two round and simple lateral lips, each with three small teeth on its internal surface; each lip bears a lateral amphid, and a pair of sub-median papillae (Figs 1B, 2B). Pharynx short, cylindrical, opening into oesophagus. Oesophagus divided into anterior muscular portion and posterior glandular portion. Excretory pore in anterior region of body, posterior to nerve ring and located at level of division of muscular and glandular oesophagus. Posterior end conical and rounded in both sexes (Figs 1F, H, 2D, F).

Figure 1.

Thubunaea leonregagnonae sp. n. A Anterior end, female, lateral view B Apical view, female C Anterior end, female, lateral view showing excretory pore and vulva D Embryonated egg, lateral view E Larvated egg, lateral view F Caudal end, male, ventral view G Caudal end, male, lateral view, caudal papillae and ornamentation not shown H Caudal end, female, lateral view. Scale bars: A 90 µm; B 20 µm; C 370 µm; D 25 µm; E 30µm; F 250 µm; G 50 µm; H 370 µm.

Description of male (based on eight specimens; the number of measurements, where different from eight, is given in parentheses): Total body length (MTBL) 4.85–8.03 mm (6.19), width at mid-body 200–300 (243). Deirids 150–185 (166; n = 7) from anterior end. Nerve ring and excretory pore 100–168 (125) and 125–295 (179, n = 6) from anterior end, respectively. Pharynx length 23–45 (33). Oesophagus total length 613–1038 (800, n = 7), muscular portion length 108–170 (128, n = 7), glandular portion length 488–913 (671, n = 7). Ratio oesophagus total length: MTBL 0.1–0.16 (0.13, n = 7). Testis elongated, distributed in zigzag from anterior intestinal portion to posterior region, near cloaca. Caudal alae well developed, bearing ventrally numerous papilliform plates. Cloaca surrounded by numerous papillae (24–28), 11–14 sessile papillae and 10–16 pedunculate papillae distributed asymmetrically in the following arrangement: ventrolateral: 4–8 pedunculate on right, 6–9 pedunculate on left side; ventral, sessile: 5–8 on right and 4–8 on left side (Figs 1F, 2E, F). Number and disposition of papillae variable with respect to cloaca, thus, precloacal, paracloacal, and postcloacal positions not established. Spicules and gubernaculum absent. Tail 50–67 (59, n = 6) long.

Description of female (based on ten gravid specimens; the number of measurements, where different from ten, is given in parentheses): Total body length (FTBL) 8.72–21.46 mm (14.61), width at mid-body 270–440 (349). Deirids 125–250 (173, n = 8) from anterior end. Nerve ring and excretory pore 100–188 (147, n = 8) and 193–343 (256, n = 6) from anterior end, respectively. Pharynx length 30–58 (41, n = 9). Oesophagus total length 853–1500 (1227, n = 7); muscular portion length 125–325 (220, n = 8), glandular portion length 703–1220 (996, n = 7); ratio oesophagus total length:FTBL 0.1–0.16 (0.14, n = 7). Didelphic, opisthodelphic, ovaries distributed in posterior region of body, uteri extended parallel along almost entire body. Vagina muscular, directed posteriorly, located in anterior region of body close to anterior end of intestine, vulva at 1130–2570 (1770) from anterior end (Fig. 1C). Ratio distance vulva to anterior end of body: FTBL 0.11–0.13 (0.12). Tail 25–30 (27, n = 8) long. Embryonated eggs occupying almost entire uterus, thick shelled with smooth surface, 39–44 (41, n = 15) long by 29–33 (31, n = 15) wide (Fig. 1D); larvated eggs located near vulva, 45–50 (48, n = 15) long by 38–40 (39, n = 15) wide (Fig. 1E).

Remarks

The family Physalopteridae is composed of three subfamilies: Thubunaeinae Sobolev, 1949, Proleptinae Schulz, 1927 and Physalopterinae Railliet, 1893 (Chabaud 1975). Thubunaeinae comprises two genera Thubunaea and Physalopteroides Wu & Liu, 1940, both of which are parasites of reptiles and are characterized by the absence of a cephalic ring, the presence of numerous caudal papillae, and an ornamented cuticle forming papillary plates distributed on the surface of the cauda in males (Chabaud 1975). These two genera differ from each other mainly by the symmetry of their cephalic structures; in Thubunaea these structures are symmetrical, while they are asymmetrical in Physalopteroides (Chabaud 1975). Some authors, for example Moravec et al. (1997), considered that the morphological features of Thubunaea and Physalopteroides have rarely been analysed using techniques such as SEM, and that these observations could provide detailed information to assess the validity of these two genera. However, to the best of our knowledge, SEM studies are still scarce in both genera, being available for only three species of Thubunaea (Moravec et al. 1997, Pazoki and Rahimian 2014, Ramallo et al. 2016) and two species for Physalopteroides (Elwasila 1990, Goswami et al. 2016). The specimens described in the present study show a symmetrical cephalic structure, as in Thubunaea.

Currently, 20 species of Thubunaea are considered as valid: one in the Afrotropical region, T. fitzsimonsi Ortlepp, 1931; five in the Nearctic region, T. cnemidophorus Babero & Matthias, 1967, T. ctenosauri Moravec, Salgado-Maldonado & Mayen-Peña, 1997, T. iguanae Telford, 1965, T. intestinalis Bursey & Goldberg, 1991 and T. leiolopismae Harwood, 1932; two in the Neotropics, T. parkeri Baylis, 1926, and T. eleodori Ramallo, Goldberg, Bursey, Castillo & Acosta, 2016; six in the Oriental region, T. aurangabadensis Deshmukh, 1969, T. brooki Deshmukh, 1969, T. hemidactylae Oshmarin & Demshin, 1972, T. mirzai Narayan, 1941, T. singhi Deshmukh, 1969, and T. syedi Deshmukh, 1969; two in the Palearctic region, T. schukurovi Annaev, 1973 and T. smogorzhewskii Sharpilo, 1966; and four species in the Saharo-Arabian region, T. baylisi Akhtar, 1939, T. dessetae Barus & Tenora, 1976, T. mobedii Pazoki & Rahimian, 2014 and T. pudica Chabaud & Golvan, 1957 (Ramallo et al. 2016).

Six of these species lack spicules, as is the case in T. leonregagnonae sp. n.: T. cnemidophorus, T. eleodori, T. fitzsimonsi, T. mobedii, T. parkeri and T. schukurovi (Table 3). Males of four of these species (T. eleodori, T. fitzsimonsi, T. parkeri and T. mobedii) are larger in body length than T. leonregagnonae sp. n. (10.25–11.16, 8.5–9, 10.5, 11.4–15.4 vs 4.85–8.03 mm, respectively). In the number of papillae, pedunculate or sessile, the new species also differs from most of these six species. Thubunaea leonregagnonae sp. n. has 10–16 pedunculate papillae and 11–14 sessile papillae, T. mobedii does not have pedunculate papillae; in contrast, T. fitzsimonsi and T. parkeri lack sessile papillae, and in this latter species the number of caudal papillae is smaller (16–20) than in the present specimens (24–28) (Table 3). Thubunaea leonregagnonae sp. n. is most similar to T. cnemidophorus, T. eleodori and T. schukurovi, however, it can be distinguished from the last two species in the number of sessile papillae: T. eleodori has ten and T. schukurovi has 16, instead of 11–14 in T. leonregagnonae sp. n. Males of T. leonregagnonae sp. n. and T. cnemidophorus can be differentiated mainly by having a different oesophagus length/MTBL ratio (0.1–0.16 vs 0.26) and by the former having a smaller body width (200–300 vs 350–390).

Figure 2.

Thubunaea leonregagnonae sp. n. Scanning electron micrographs. A Anterior end, male, lateral view showing deirid (D) B Apical view, female, showing sub-median papillae (P) and amphids (A) C Deirid, lateral view D Posterior end, female, ventrolateral view E Posterior end, male, ventral view F Caudal end, male, ventral view. Scale bars: A 50 µm; B 10 µm; C 2.5 µm; D 50 µm; E 100 µm; F 50 µm.

Table 3.

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Morphological characters of Thubunaea spp. lacking spicules in males. Measurements in micrometres, unless otherwise indicated.

Species	T. cnemidophorus Babero & Matthias, 1967	T. eleodori Ramallo, Goldberg, Bursey, Castillo & Acosta, 2016	T. fitzsimonsi Ortlepp, 1931	T. mobedii Pazoki & Rahimian, 2014	T. parkeri Baylis, 1926	T. schukurovi Annaev, 1973	Thubunaea leonregagnonae sp. n.
Source	Babero and Matthias (1967)	Ramallo et al. (2016)	Ortlepp (1931)	Pazoki and Rahimian (2014)	Baylis (1926)	Annaev (1973)	Present study
Type host	Aspidoscelis tigris (Baird & Girard) (Teiidae)	Liolaemus eleodori Cei, Etheridge & Videla (Liolaemidae)	Meroles squamulosus (Peters) (Lacertidae)	Laudakia nupta nupta (De Filippi) (Agamidae)	Microlophus occipitalis (Peters) (Tropiduridae)	Ablepharus deserti Strauch (Scincidae)	Sceloporus pyrocephalus Cope (Phrynosomatidae)
Country	USA	Argentina	South Africa	Iran	Peru	Turkmenistan	Mexico
Biogeographical realm	Nearctic	Neotropical	Afrotropical	Saharo-Arabian	Neotropical	Palearctic	Nearctic
MTBL (mm)	5.7–6.6	10.25–11.16	8.5–9.0	11.4–15.4	10.5	7.8	4.85–8.03
MTBW	350–390	360	290–330	190–330	300–340	300	200–300
PP	14–16	12	29–31	0	16–20	12	10–16
SP	12	10	0	23–37	0	16	11–14
OE/MTBL	0.26^†	0.12	0.11	0.12	0.1	0.15	0.1–0.16
Eggs	38–45 × 23–30			44–45 × 36–39	58–63 × 48–53		45–50 × 38–40
Eggs	(38 x 23)	(48 x 41)	(45 x 38)	(48 x 38)	(60 x 50)	(43 x 33)

Discussion

Many authors have argued that the inventory of the parasite fauna of host species is of critical importance in biodiversity management and conservation efforts (Brooks and Hoberg 2000, Brooks and McLennan 2002, Funks and Richardson 2002). Parasite studies help to reveal other biological aspects of the hosts such as their natural history and ecology. The close link between parasites and their hosts causes these studies to have a cascade effect on our knowledge of the biology of the interaction between host and parasite, as well as with the environment in which this association developed. For this reason, helminthological studies on hosts distributed in areas with high potential for endemism, such as in the present study, are highly relevant for understanding the ecology and evolution of parasite-host interactions.

Presently, for S. pyrocephalus, a single study was conducted, evaluating parasite load in conjunction with hormone concentration (Calisi et al. 2008). In this study, only nematodes and cestode larvae were found, without, however, identifying these to species level.

In the present study, nine helminth taxa were found parasitizing S. pyrocephalus: two tapeworms of the order Cyclophyllidea (Mesocestoides sp. and Oochoristica sp.), one nematode of the order Ascaridida (S. similis), three of the order Rhabditida (P. ayotzinapaensis. P. tikuinii, and Parapharyngodon sp.), and three of the order Spirurida (Physalopterinae gen. sp., S. scelopori and T. leonregagnonae sp. n.). Most of these taxa coincide with previous reports on the helminth fauna from lizards in Mexico (Caballero 1938, Telford 1965, Goldberg et al. 1996, Moravec et al. 1997, Goldberg et al. 2003, Paredes-León et al. 2008). Parapharyngodon ayotzinapaensis, P. tikuinii and T. leonregagnonae sp. n. have been recorded as specific nematode species for this lizard. The current results increase from 35 to 40 the number of helminths recorded as parasites of Sceloporus spp. and from 17 to 18 the number of species of this lizard genus for which parasite records are available (Paredes-León et al. 2008).

Oochoristica sp., P. ayotzinapaensis, P. tikuinii, Parapharyngodon sp., S. scelopori, S. similis, and T. leonregagnonae sp. n. use S. pyrocephalus as a definitive host, and Mesocestoides sp. and Physalopterinae gen. sp. were recorded as larval stages. Mesocestoides sp. is a common metacestode found in the body cavity and mesentery of amphibians and reptiles, which serve as paratenic hosts, with carnivorous mammals being the definitive hosts (Santoro et al. 2012). Specimens of Physalopterinae gen. sp. were found in the stomach and large intestine; species belonging to this subfamily are adult parasites of amphibians, reptiles and mammals, so their presence in S. pyrocephalus was probably a result of a recent recruitment.

It has been suggested that reptiles that use a passive feeding strategy (i.e. sit-and-wait) have a less diverse and less complex helminth fauna than those with an active searching behaviour (e.g. widely foraging) (Roca 1999), and that these foraging strategies are directly related to the diet of the lizards, with a passive strategy used by predominantly herbivorous lizards and an active search used by carnivorous ones. Nematodes with a direct life cycle, such as pinworms (Oxyurida: Pharyngodonidae), best reveal the differences between herbivore and carnivore hosts. Within the Pharyngodonidae, a family of Oxyuroidea that are characteristic parasites of amphibians and reptiles, are two evolutionary lineages that show a diversification that mirrors that of their hosts' diets. (Roca 1999). Some genera of Pharyngodonidae infect only carnivorous saurian reptiles: Parapharyngodon, Spauligodon Skrjabin, Schikhobalova & Lagodovskaja, 1960, Skrjabinodon, Pharyngodon and Parathelandros Baylis, 1930; while the second linage is composed of pharyngodonid parasites of herbivorous iguanids and testudines: Tachygonetria Wedl, 1862, Mehdiella Seurat, 1918, Alaeuris Seurat, 1918, Thaparia Ortlepp, 1933, Ortleppnema Petter, 1966, Ozolaimus Dujardin, 1845, Travassozolaimus Vigueras, 1938 and Mamillomacracis Dosse, 1939. Given the particular species of Oxyuroidea found in S. pyrocephalus, along with the presence of S. similis, a typical nematode found in carnivorous reptiles (Núñez 2005), it can be inferred that this lizard is mainly carnivorous. The remaining taxa of helminths found in the present study, including the nematodes T. leonregagnonae sp. n. and S. scelopori, have an indirect life cycle, in which beetles and ants are probably acting as intermediate hosts. Studies in other species of Sceloporus have determined that termites are an important food source for S. gadoviae Boulenger, S. horridus Wiegmann, and S. jalapae Günther (Serrano-Cardozo et al. 2008); hence, termites could likely be the intermediate hosts of the heteroxenous parasites found in S. pyrocephalus.

Since five of the nine parasite taxa recorded for S. pyrocephalus have an indirect life cycle, with arthropods as intermediate hosts, diet might be the predominant factor structuring the helminth fauna in this lizard. This opposes the idea proposed by Aho (1990), who found that most of the parasite species that inhabit the intestine of amphibians and reptiles, are nematodes with a direct life cycle. Studies assessing the helminth fauna associated with Mexican reptiles are of great value to have a better understanding of the factors that influence the ecological dynamics within helminth communities and to establish comparisons between Nearctic and Neotropical populations of hosts.

Acknowledgments

The first author thanks CONACyT for the scholarship granted to obtain his Master’s degree at the Posgrado en Ciencias Biológicas, UNAM. We thank Erick Alejandro García-Trejo and Eduardo Villalobos Segura for reviewing a preliminary version of the manuscript. Thanks to Jonathan A. Campbell, Carl J. Franklin, and Leticia Ochoa for the catalogue number of lizard specimens, and to Berenit Mendoza-Garfias for her technical support with the SEM micrographs. Funding for this study was obtained from the Project “The amphibians and reptiles and their parasites of Mexico, a megadiverse country” (National Science Foundation DEB-01613802) to Jonathan A. Campbell and Virginia León-Règagnon. We thank to Yuriy Kuzmin and an anonymous reviewer who have provided important suggestions to improve the manuscript.

References

Aho JM (1990) Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes. In: Esch GW, Bush AO, Aho JM (Eds) Parasite communities: patterns and processes.Chapman and Hall, London, 157–195. https://doi.org/10.1007/978-94-009-0837-6_7

Annaev D (1973) Thubunaea schukurovi n. sp. (Physalopteridae, Nematoda) from lizards in Turkmenia. Izvestia Akademii Nauk Turkmenskoi SSR 1: 72–75. [In Russian]

Arizmendi-Espinosa MA, Garcia-Prieto L (2005) A new species of Oochoristica (Eucestoda: Cyclophyllidea) parasite of Ctenosaura pectinata (Reptilia: Iguanidae) from Oaxaca, Mexico. Journal of Parasitology 91: 99–101. http://dx.doi.org/10.1645/GE-337R

Babero BB, Matthias D (1967) Thubunaea cnemidophorus n. sp., and other helminths from lizards, Cnemidophorus tigris, in Nevada and Arizona. Transactions of the American Microscopical Society 86: 173–177. https://doi.org/10.2307/3224688

Baylis HA (1926) On a new species of the nematode genus Thubunaea. Annals and Magazine of Natural History 17: 361–364. https://doi.org/10.1080/00222932608633527

Brooks DR, Hoberg EP (2000) Triage for the biosphere: the need and rationale for taxonomic inventories and phylogenetic studies of parasites. Comparative Parasitology 68: 1–25.

Brooks DR, McLennan DA (2002) The nature of diversity: an evolutionary voyage of discovery. University of Chicago Press, Chicago, 676 pp. https://doi.org/10.7208/chicago/9780226922478.001.0001

Brooks DR, Pérez-Ponce de León G, García-Prieto L (1999) Two new species of Oochoristica Lühe, 1898 (Eucestoda: Cyclophyllidea: Anoplocephalidae: Linstowiinae) parasitic in Ctenosaura spp. (Iguanidae) from Costa Rica and Mexico. Journal of Parasitology 85: 893–897. https://doi.org/10.2307/3285828

Bursey CR, Goldberg SR (1991) Thubunaea intestinalis n. sp.(Nematoda: Spiruroidea) from Yarrow’s spiny lizard, Sceloporus jarrovii (Iguanidae), from Arizona, USA. Transactions of the American Microscopical Society 110: 269–278. https://doi.org/10.2307/3226661

Bursey CR, Goldberg SR (2015) Description of a new species of Parapharyngodon (Nematoda: Pharyngodonidae) from Mexico with a list of current species and key to species from the Panamanian region. Journal of Parasitology 101: 374–381. https://doi.org/10.1645/13-460.1

Bursey CR, Goldberg SR, Telford SR Jr (2003) Strongyluris panamaensis n. sp. (Nematoda: Heterakidae) and other helminths from the lizard, Anolis biporcatus (Sauria: Polychrotidae), from Panamá. Journal of Parasitology 89: 118–123. http://dx.doi.org/10.1645/0022-3395(2003)089[0118:SPNSNH]2.0.CO;2

Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83: 575–583. https://doi.org/10.2307/3284227

Caballero CE (1937) Nemátodos de algunos vertebrados del Valle del Mezquital, Hidalgo. Anales del Instituto de Biología, Universidad Nacional Autónoma de México 8: 189–200.

Caballero CE (1938) Nematodes parasites des reptiles de Mexique. Annales de Parasitologie Humaine et Compareé 16: 327–333. https://doi.org/10.1051/parasite/1938164327

Caballero CE (1951) Estudios helmintológicos de la región oncocercosa de México y de la República de Guatemala. Nematoda. 6ª parte. Y algunas consideraciones en torno a los géneros Onchocerca Diesing, 1841 y Acanthospiculum Skrjabin y Schikobalowa, 1948. Anales del Instituto de Biología, Universidad Nacional Autónoma de México 22: 141–158.

Caballero-Rodríguez G (1971) Contribución al conocimiento de los nemátodos que parasitan a los reptiles de México. II. Sobre una nueva fisalóptera parásita de iguánidos (Sceloporus torquatus torquatus Wiegmann, 1828). Revista de Biología Tropical 19: 165–179.

Calisi RM, Malone JH, Hews DK (2008) Female secondary coloration in the Mexican boulder spiny lizard is associated with nematode load. Journal of Zoology 276: 358–367. https://doi.org/10.1111/j.1469-7998.2008.00499.x

Chabaud AG (1975) No. 3. Keys to genera of the order Spirurida. Part 1. Camallanoidea, Dracunculoidea, Gnathostomatoidea, Physalopteroidea, Rictularioidea and Thelazioidea. In: Anderson RC, Chabaud AG, Willmott S (Eds) CIH Key to the nematode parasites of vertebrates.CAB International, Wallingford, 29–58.

Cid del Prado VI (1971) Estudio taxonómico de algunos nemátodos parásitos de reptiles de México. B.S. Thesis, Facultad de Ciencias, Universidad Nacional Autónoma de México, Mexico City, 102 pp.

Elwasila M (1990) Physalopteroides tarentolae n. sp. (Nematoda: Physalopteridae) from the gecko Tarentola annularis in the Sudan. Systematic Parasitology 15: 121–125. https://doi.org/10.1007/BF00009989

Flores-Barroeta L (1955) Céstodos de vertebrados. II. Revista Ibérica de Parasitología 15: 115–134.

Flores-Barroeta L, Hidalgo-Escalante E (1960) Céstodos de vertebrados. VII. In: Bravo-Hollis M, Zerecero C, Flores-Barroeta L, Hidalgo-Escalante E, Winter HA (Eds) Libro Homenaje al Dr.Eduardo Caballero y Caballero. Secretaría de Educación Pública, Instituto Politécnico Nacional, Mexico City, 357–376.

Flores-Villela O, García-Vázquez U (2014) Biodiversidad de reptiles en México. Revista Mexicana de Biodiversidad 85: S467–S475. http://dx.doi.org/10.7550/rmb.43236

Funks VA, Richardson KS (2002) Systematic data in biodiversity studies: use it or lose it. Systematic Biology 51: 303–316. https://doi.org/10.1080/10635150252899789

Garduño-Montes de Oca EU, Mata-López R, León-Règagnon V (2016) Two new species of Parapharyngodon parasites of Sceloporus pyrocephalus, with a key to the species found in Mexico (Nematoda, Pharyngodonidae). ZooKeys 559: 1–16. https://doi.org/10.3897/zookeys.559.6842

Goldberg SR, Bursey CR (1991) Gastrointestinal helminths of the Mexican lizards, Phrynosoma braconnieri and Phrynosoma taurus (Iguanidae). Southwestern Naturalist 36: 365–368. https://doi.org/10.2307/3671694

Goldberg SR, Bursey CR (2000) Helminths of Mexican lizards: geographical distribution. In: Salgado-Maldonado G, García-Aldrete AN, Vidal-Martínez VM (Eds) Metazoan parasites in the Neotropics: a systematic and ecological perspective.Universidad Nacional Autónoma de México, Instituto de Biología. D. F., Mexico, 175–191.

Goldberg SR, Bursey CR, Bezy RL (1996) Gastrointestinal helminthes of Yarrow´s spiny lizard, Sceloporus jarrovii (Phrynosomatidae) in Mexico. American Midland Naturalist 135: 299–309. https://doi.org/10.2307/2426713

Goldberg SR, Bursey CR, Camarillo JL (2003) Gastrointestinal helminths of seven species of sceloporine lizards from Mexico. Southwestern Naturalist 48: 208–217. https://doi.org/10.1894/0038-4909(2003)048<0208:GHOSSO>2.0.CO;2

Goswami U, Chaudhary A, Verma C, Singh HS (2016) Molecular and ultrastructure characterization of two nematodes (Thelandros scleratus and Physalopteroides dactyluris) based on ribosomal and mitochondrial DNA sequences. Helminthologia 53: 165–171. https://doi.org/10.1515/helmin-2016-0013

Guillén-Hernández S, García-Prieto L, Arizmendi-Espinosa MA (2007) A new species of Oochoristica (Eucestoda: Cyclophyllidea) parasite of Ctenosaura oaxacana (Reptilia: Iguanidae) from Mexico. Journal of Parasitology 93: 1136–1139. http://dx.doi.org/10.1645/GE-1118R.1

Jiménez FA, León-Règagnon V, Pérez-Ramos E (2008) Two new species of Parapharyngodon (Oxyuroidea: Pharyngodonidae) from the enigmatic Bipes canaliculatus and Bipes tridactylus (Squamata: Bipedidae). Revista Mexicana de Biodiversidad 79: 1136–1206. http:// www.scielo.org.mx/pdf/rmbiodiv/v79sago/v79sagoa16.pdf

Kabilov TK (1980) The life cycle of Abbreviata kazachstanica. Parazitologiia 14: 263–270.

Lamothe-Argumedo R (1997) Manual de técnicas para preparar y estudiar los parásitos de animales silvestres. AGT, Mexico, 43 pp.

Lee SH (1957) The life cycle of Skrjabinoptera phrynosoma (Ortlepp) Schulz, 1927 (Nematoda: Spiruroidea), a gastric nematode of Texas horned toads, Phrynosoma cornutum. Journal of Parasitology 43: 66–75. https://doi.org/10.2307/3274761

Moravec F, Salgado-Maldonado G, Mayén-Peña E (1997) Thubunaea ctenosauri sp. n. (Nematoda: Physalopteridae) from the iguanid lizard Ctenosaura pectinata and other lizard helminths from Mexico. Journal of the Helminthological Society of Washington 64: 240–247. http://bionames.org/bionames-archive/issn/1049-233X/64/240.pdf

Núñez VS (2005) Dieta de la lagartija Sceloporus pyrocephalus. Bachelor Thesis. Universidad Muchoacana de San Nicolás de Hidalgo. Morelia, Michoacán. México, 49 pp.

Ortlepp RJ (1931) Thubunaea fitzsimonsi sp. n., a fourth species of the genus Thubunaea Seurat, 1914. Journal of the South African Veterinary Medical Association 2: 128–131. https://journals.co.za/content/savet/2/2/AJA00382809_2117

Paredes-León R, García-Prieto L, Guzmán-Cornejo C, León-Règagnon V, Pérez TM (2008) Metazoan parasites of Mexican amphibians and reptiles. Zootaxa 1904: 1–166. http://www.realitat.com/websites/zoologia/zoo_08/tecnicos_s_853645/archivos/Metazoan%20parasites.pdf

Pazoki S, Rahimian H (2014) New species of Spauligodon Skrjabin, Schikhobalova & Lagodovskaja, 1960 and Thubunea Seurat, 1914 (Nematoda) from the gastro-intestinal tract of lizards in Iran. Systematic Parasitology 89: 259–270. https://doi.org/10.1007/s11230-014-9527-y

Petri LH (1950) Life cycle of Physaloptera rara Hall and Wigdor, 1918 (Nematoda: Spiruroidea) with the cockroach, Blatella germanica, serving as the intermediate host. Transactions of the Kansas Academy of Science 53: 331–337. https://doi.org/10.2307/3626145

Ramallo G, Goldberg S, Bursey C, Castillo G, Acosta JC (2016) Thubunaea eleodori sp. nov. (Nematoda: Physalopteridae) from Liolaemus eleodori (Sauria: Liolaemidae) from Argentina. Parasitology Research 16: 293–297. https://doi.org/10.1007/s00436-016-5290-0

Roca V (1999) Relación entre las faunas endoparásitas de reptiles y su tipo de alimentación. Revista Española de Herpetología 13: 101–121. http://www.lacerta.de/AS/Bibliografie/BIB_1784.pdf

Rudolphi CA (1819) Entozoorum synopsis, cui accedunt mantissa duplex et indices locupletissimi. Sumtibus Augusti Rücker, Berolini, 811 pp. https://doi.org/10.5962/bhl.title.9157

Santoro M, Aznar EJ, Mattiucci S, Kinsella JM, Pellegrino F, Cipriani P, Nascetti G (2012) Parasite assemblages in the Western whip snake Hierophis viridiflavus carbonarius (Colubridae) from southern Italy. Journal of Helminthology 87: 1–9. https://doi.org/10.1017/S0022149X12000338

Schell SC (1952) Studies on the life cycle of Physaloptera hispida Schell (Nematoda: Spiruroidea) a parasite of the cotton rat (Sigmodon hispidus littoralis Chapman). Journal of Parasitology 38: 462–472. https://doi.org/10.2307/3273926

Serrano-Cardozo VH, Lemos-Espinal JA, Smith GR (2008) Comparative diet of three sympatric Sceloporus in the semiarid Zapotitlán Valley, México. Revista Mexicana de Biodiversidad 79: 427–434. http://www.scielo.org.mx/pdf/rmbiodiv/v79n2/v79n2a17.pdf

Stunkard HW (1938) Parasitic flatworms from Yucatan. Publications of the Carnegie Institution of Washington 491: 33–50. http://hdl.handle.net/11154/162411

Telford SR (1965) A new species of Thubunaea (Nematoda: Spiruroidea) from California lizards. Japanese Journal of Experimental Medicine 35: 111–114.

Uetz P, Freed P, Hošek J (Eds) (2016) The Reptile Database. http://www.reptile-database.org [accessed May 11, 2017]

Velarde-Aguilar MG, Mata-López R, Guillén-Hernández S, León-Règagnon V (2015) Parapharyngodon n. spp. (Nematoda: Pharyngodonidae) parasites of hylid frogs from Mexico and review of species included in the genus. Journal of Parasitology 101: 212–230. https://doi.org/10.1645/13-328.1