Parapharyngodon ayotzinapaensis, Garduno-Montes de Oca, Edgar Uriel, Mata-Lopez, Rosario & Leon-Regagnon, Virginia, 2016

Garduno-Montes de Oca, Edgar Uriel, Mata-Lopez, Rosario & Leon-Regagnon, Virginia, 2016, Two new species of Parapharyngodon parasites of Sceloporuspyrocephalus, with a key to the species found in Mexico (Nematoda, Pharyngodonidae), ZooKeys 559, pp. 1-16 : 2-4

Taxon classification Animalia Oxyurida Pharyngodonidae

Parapharyngodon ayotzinapaensis sp. n. Figs 1 A–E; 2 A–H

Type material.

Holotype, male, CNHE 9432. Allotype, female, CNHE 9433. Paratypes (4 males, 7 females), CNHE 9434-9438.

Etymology.

The species is named in honor of the 43 missing students from "Escuela Normal Rural Raúl Isidro Burgos" in Ayotzinapa, Guerrero, Mexico; in solidarity with their families and the Mexican people.

Diagnosis.

Robust, small and white fusiform nematodes, males smaller than females. Cuticle with prominent transverse striations along the whole body except tail. Triangular oral opening surrounded by three simple lips in males and bilobed in females, in both sexes ventrolateral lips have an amphid each one, in females it is located on the dorsal lobe. Within buccal cavity, both sexes have three transverse plates, bilobed in males and complete in females. Esophageal bulb with sclerotized apparatus. Excretory pore evident, it is located at level of posterior edge of esophageal bulb. A vesicular body surrounds excretory duct. Males with lateral alae covering the last third of body, females lacking lateral alae. Males without caudal alae. Four pairs of caudal papillae. Caudal filament sub-terminal and directed dorsally in males. Females with a conical posterior end. Vulva located at middle region. Eggs no shown alae, with a punctuated shell and subpolar operculum, embryo in early stage of cleavage.

Description of male.

Distinctly truncate posterior end (Fig. 1E), total body length 2.72-3.92 (3.458 ± 0.458, n = 5), maximum width 0.6-1.88 (1 ± 0.505, n = 5) at middle region. Cuticle with wide transverse striae 0.05-0.08 (0.062 ± 0.011, n = 5) maximum width at middle region. Triangular oral opening surrounded by three simple lips at whose internal bases are located three transverse bilobed plates, ventrolateral lips with one amphid each one (Fig. 2D). Esophagus total length 0.7-0.84 (0.79 ± 0.054, n = 5) and maximum width 0.04-0.06 (0.05 ± 0.01, n = 5), esophageal bulb length 0.12-0.17 (0.148 ± 0.023, n = 5) and width 0.13-0.16 (0.146 ± 0.013, n = 5). Nerve ring and excretory pore 0.1-0.24 (0.172 ± 0.064, n = 4) and 0.74-1.39 (1.046 ± 0.237, n = 5) from anterior end, respectively. Testis extends from middle body region to level of anterior end of intestine. Lateral alae start abruptly from level of the beginning of third caudal region of body (Fig. 1E). The left one at 2.24-3.01 (2.573 ± 0.395, n = 3), and the right one at 2.31-2.88 (2.565 ± 0.253, n = 4) from anterior end, both with a maximum width of 0.06-0.07 (0.062 ± 0.005, n = 4); extending to posterior end of body, the left one at 0.02-0.07 (0.046 ± 0.025, n = 3) and the right one at 0.03-0.09 (0.056 ± 0.023, n = 5) from the base of corresponding paracloacal papillae. Four pairs of caudal papillae distributed as follows: one precloacal pedunculate, one paracloacal pedunculate, one lateral sessile at the central lobe apex of postcloacal lip and one mammilliform at 0.06-0.07 (0.065 ± 0.006, n = 4) from posterior end of caudal filament (Fig. 2A and B). Top of pedunculate and mammilliform papillae in a rosette-like structure (Fig. 2A, B and E). Echinate precloacal lip with rough appearance, at base of posteriorly directed finger-like ornamentation, which vary in simple or bifurcate outgrowths disposition (Figs 1B; 2B). In SEM pictures morphology is distinguished as follows: cloacal lip rise up from anterior cloacal edge, at both end sides it has a rough thickening region longer that remainder of lip (1 and 5 in Fig. 2B), adjacent to these, at both sides of lip and towards central axis of body, there are finger-like outgrowths that start from rough regions (2 and 4 in Fig. 2B). On the central axis of body is located a rough region (3 in Fig. 2B) upon which are situated finger-like outgrowths, at each side of this region other finger-like outgrowths are situated. Posterior cloacal lip is divided into three lobes, the middle one is more developed than lateral lobes, it is 0.03-0.05 (0.04 ± 0.008, n=4) length and has a pair of tiny simple papillae (Fig. 2C). Caudal filament 0.09-0.1 (0.093 ± 0.006, n = 3) length. Phasmids situated on caudal filament base laterally. Spicule length 0.11-0.13 (0.12 ± 0.01, n = 3) 3.614% of body length, distal end obtuse and thinnest than proximal (Fig. 1D).

Description of female.

Round anterior end and conical posterior end (Fig. 1A), total body length 6.41-9.32 (7.45 ± 1.149, n = 8) and maximum width 0.76-1.26 (0.94 ± 0.189, n = 8) at middle body region. Cuticle with wide transverse striae 0.07-0.09 (0.08 ± 0.01, n = 8) maximum width at esophageal bulb level. Triangular oral opening surrounded by three bilobed lips whose internal base are located three transverse complete plates, ventrolateral lips with one amphid each one located at dorsal lobe (Fig. 2F). Esophagus total length 1.17-1.35 (1.269 ± 0.073, n = 8) and maximum width 0.07-0.09 (0.076 ± 0.007, n = 8), esophageal bulb length 0.15-0.21 (0.177 ± 0.019, n = 7) and width 0.21-0.28 (0.24 ± 0.024, n = 7). Nerve ring and excretory pore 0.15-0.21 (0.181 ± 0.023, n = 8) and 1.71-2.4 (1.937 ± 0.237, n = 8) from anterior end, respectively. Sclerotized vulva at 2.95-4.13 (3.45 ± 0.396, n = 8) from anterior end. Vagina transversely directed and posteriorly flexed to posterior region of body. Didelphic, prodelphic, ovaries reach esophagus region coiling around prebulbar esophagus. Uterus reach caudal region in gravid individuals. Anus 0.4-0.48 (0.435 ± 0.039, n = 6) from posterior end. Phasmids 0.14-0.25 (0.204 ± 0.042, n = 8) from posterior end, located laterally at the base of the conical tail (Fig. 2F). Tail 0.2-0.26 (0.237 ± 0.026, n = 8) length. Eggs containing embryo in early stage of cleavage, oval, without alae, asymmetric, slightly flattened on one side and convex on the other side in lateral view, 0.07-0.09 (0.08 ± 0.006, n = 16) length by 0.03-0.05 (0.04 ± 0.005, n=16) width, shell with pores that cross the uppermost layer, radial striations in lateral view, subpolar operculum without pores (Figs 1C; 2H).

Distribution.

Técpan de Galeana, Guerrero, Mexico (coordinates, see Table 1; elevation 22 m).

Biology.

Nematode species parasite of the intestine of Sceloporus pyrocephalus Cope, collected on July 6, 2005.

Remarks.

Parapharyngodon ayotzinapaensis sp. n. is the 79th species assigned to Parapharyngodon and the 48th valid species of the genus ( Velarde-Aguilar et al. 2015; Bursey and Goldberg 2015). It is distinguished from the other Parapharyngodon species by a combination of characters including the possession of 4 pairs of caudal papillae, an echinate anterior cloacal lip, lateral alae covering the last third of body, spicule length representing 3.614% of body length, prebulbar ovaries coiling around prebulbar esophagus and eggs with punctuated shell and without alae. Of the 47 valid species before this study, 12 species have cloacal papillar arrangement similar to Parapharyngodon ayotzinapaensis (four pairs of caudal papillae: one precloacal, one paracloacal, one at postcloacal lip and one at caudal filament), as well as echinate precloacal lip and lateral alae, namely: Parapharyngodon adramitana Adamson & Nasher, 1984, Parapharyngodon almoriensis (Karve, 1949) Freitas, 1957, Parapharyngodon anomalus Hobbs, 1996, Parapharyngodon brevicaudatus Bogdanov & Markov,1955, Parapharyngodon colonensis Bursey, Goldberg & Telford, 2007, Parapharyngodon dolgieli (Markov & Bogdanov, 1965) Adamson & Nasher, 1984, Parapharyngodon echinatus (Rudolphi, 1819) Freitas, 1957, Parapharyngodon grenadaensis Bursey, Drake, Cole, Sterner, Pinckney & Zieger, 2013, Parapharyngodon margaritiferi Hering-Hagenbeck, 2001, Parapharyngodon meridionalis (Chabaud & Brygoo, 1962) Adamson, 1981, Parapharyngodon micipsae (Seurat, 1917) Freitas, 1957 and Parapharyngodon rousseti (Tcheprakoff, 1966) Adamson & Nasher, 1984. Only 2 of these species ( Parapharyngodon grenadaensis and Parapharyngodon colonensis ) shares with the new species the egg shell punctuated and prebulbar ovaries in females; however, these two species differ in several morphological features with Parapharyngodon ayotzinapaensis sp. n.: Parapharyngodon grenadaensis and Parapharyngodon colonensis have three bilobed lips, which are simple in Parapharyngodon ayotzinapaensis ; lateral alae extension covers from nerve ring level to precloacal papillae in Parapharyngodon grenadaensis and Parapharyngodon colonensis , meanwhile in Parapharyngodon ayotzinapaensis begins abruptly at last third of caudal region ending before paracloacal papillae. Finally, spicule length/body length ratio is greater in Parapharyngodon grenadaensis (4.488%) and Parapharyngodon colonensis (3.765%) than in Parapharyngodon ayotzinapaensis (3.614%). Therefore, we consider Parapharyngodon ayotzinapaensis to represent a new species, the 10th recorded in Mexico ( Bursey and Goldberg 2005, Bursey et al. 2013, Velarde-Aguilar et al. 2015, Bursey and Goldberg 2015).