Bidigiticauda vivipara Chitwood

Bidigiticauda vivipara Chitwood

Site of infection: Small intestine

Host: Glossophaga mutica

Locality: Campamento Bugambilias (21°39’41.2” N, 106°36’58.3” W, 164 MASL), Islas Marías , Nayarit

Prevalence and intensity: 33.3% (1/3) and 131

Specimens deposited: CNHE 12131

GenBank accession numbers: PQ476176, PQ476177

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Redescription: Based on 11 males, 11 females, and six third-stage larvae. Nematodes with cephalic vesicle ( Figures 4A View FIGURE 4 , 5A View FIGURE 5 ), usually wider than long ( Figure 4A View FIGURE 4 ). Presence of four double cephalic papillae, two dorsolateral and two ventrolateral, as well as two amphids ( Figure 5B View FIGURE 5 ). Esophageal tooth present ( Figure 4A View FIGURE 4 ). Male and female lack longitudinal ridges ( Figures 4B, C View FIGURE 4 , 5A, C, F View FIGURE 5 ).

Males: Body length 3746 (3480‒4250) and width at midbody 124 (100‒140). Cephalic vesicle 103 (85‒118) long and 117 (95‒135) wide. Nerve ring, excretory pore and deirids situated at 199 (175‒220), 306 (235‒368), and 301 (232‒368) from anterior end, respectively. Esophagus 319 (280‒370) long. Caudal bursa subsymmetrical ( Figures 4D View FIGURE 4 , 5D View FIGURE 5 ). Rays 2, 3, and 4 arising independently, ray 4 slightly separated from ray 3. Rays 5 and 6 long, originating from common trunk ( Figure 4D View FIGURE 4 ). Dorsal ray long, divided at its distal third into 2 branches ( Figure 4D View FIGURE 4 ). In two specimens, bursal rays presented variations: right rays 4 and 5 fused ( Figure 4E View FIGURE 4 ), left ray 2 and 3 fused and dorsal ray’s right branch long ( Figure 4F View FIGURE 4 ). Spicules subequal, alate, 182 (160‒200) long with sharp tips enclosed in a spatulate membrane ( Figure 4H View FIGURE 4 ). Ratio spicule length/body length: 4.8% (4‒5.3%). Gubernaculum absent. Genital cone with dorsal lip more developed than ventral lip ( Figure 5D View FIGURE 5 ); papillae 7 situated on dorsal lip ( Figure 5E View FIGURE 5 ).

Females: Body length 6330 (5480–7670) and width at midbody 186 (170–200). Cephalic vesicle 111 (90–130) long and 145 (115–170) wide. Nerve ring, excretory pore, and deirids situated at 201 (140–245), 291 (228–365), and 290 (220–380) from anterior end, respectively. Esophagus 315 (240–360) long ( Figure 4A View FIGURE 4 ). Viviparous. Didelphic. Vulva situated at 3093 (2500–3750) from caudal extremity ( Figure 4I View FIGURE 4 ). Ratio distance vulva-posterior extremity/ body length 48.9% (39.3–55.6%). Anus 245 (180–300) from caudal extremity ( Figure 4G View FIGURE 4 ). Tail elongated, subcylindrical with two small terminal digitiform processes ( Figures 4G View FIGURE 4 , 5F View FIGURE 5 ).

Third-stage larvae: Body length 538 (510–608) and width 35 (35–37). Esophagus 176 (165–200) long. Anterior end showing rod-like structure, 11 (10–12) long. Nerve ring and excretory pore situated at 76 (70–80) and 91 (70– 110) from apex, respectively ( Figure 4J View FIGURE 4 ). Genital primordium and anus located 185 (138–512205) and 48 (45–50) from posterior extremity, respectively ( Figure 4J View FIGURE 4 ).

Remarks: The bursal pattern and dorsal lobe of the male specimens from Nayarit agrees with the brief description of B. vivipara provided by Chitwood (1938) and the redescription by Caballero-Deloya (1971). In Mexico, B. vivipara has been reported from A. jamaicensis in Yucatan ( Chitwood 1938), A. lituratus in Guerrero (Caballero-Deloya 1971), and A. jamaicensis and A. lituratus in Chiapas ( Ubelaker et al. 1977). However, the present specimens were smaller than those reported by Chitwood, (1938) and Caballero-Deloya (1971) (male body length 3480‒4250 vs 5120 and vs 10384‒10554; female body length 5480–7670 vs 8020–8060 and vs 11932‒11967). Similarly, the spicule length of our specimens was smaller than those described by Chitwood and Caballero-Deloya (160–200 vs 256–270 and vs 235–252). Nevertheless, the ratio spicule length/body length was similar between the Nayarit and Yucatan specimens (4–5.3 vs 5). In contrast, this ratio was longer compared to Caballero-Deloya’s material (4–5.3 vs 2.2–2.4). The difference in size among these B. vivipara isolates may be attributed to their occurrence in different host species ( A. jamaicensis , A. lituratus , and G. mutica ), as well as the fact that each morphological description is based on nematodes isolated from a single individual host. Furthermore, Chitwood’s original description was based on one male and two females, whereas Caballero-Deloya redescribed the species without specifying the number of specimens measured, although he collected 49 specimens (Caballero-Deloya 1971). Based on these data, it is difficult to determine at which point along this morphological and morphometrical continuum a B. vivipara isolate may be considered a different species. Further studies incorporating morphological and molecular data from several host species and geographical locations are necessary to investigate whether B. vivipara is a species complex.

The genus Bidigiticauda contains two other species: Bidigiticauda embryophilum (Freitas & Dobbin) described from Glossophaga soricina (Pallas) in Brazil, and Bidigiticauda serrafreirei de Oliveira Simões, Fraga-Neto, Vilar Maldonado Júnior & Vilela described from Artibeus planirostris (Spix) , in Brazil. Bidigiticauda embryophilum differs from B. vivipara by having rays 5 and 6 arising independently, the branches of the dorsal ray not reaching the edge of the caudal bursa, and deirids situated posterior to the esophagus-intestinal junction ( Vicente et al.,1997). Bidigiticauda serrafreirei can be distinguished from B. vivipara by the bifurcation of the dorsal ray in the middle of the trunk and the distance of the excretory pore from the anterior end that is longer (de Oliveira Simões et al., 2019).

The new record of B. vivipara from G. mutica in Nayarit expands the host and geographical range of this nematode in the country.